Patterns of Parasitism by Trybliographa rapae (Westw.), a Cynipid Parasitoid of the Cabbage Root Fly.
by
Thomas Hefin Jones, B.Sc.
A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College of Science and Technology.
Dept. of Pure and Applied Biology Imperial College, Si!wood Park, Ascot, Berkshire June 1986 -2-
ABSTRACT
This study aimed to explore the interaction between the cabbage root fly, Delia radicum (L.) (Diptera:Anthomyiidae), an important pest of cruciferous crops, and a cynipid parasitoid Trybliographa rapae (Westw.). Aspects of the parasitoid's behaviour were explored and compared under both laboratory and field conditions.
Information was gathered concerning the longevity and fecundity of the parasitoid. Behavioural studies showed that T.rapae was arrested on areas containing potential hosts by chemical stimuli emanating from infested Brassica plants.
Trybliographa rapae exhibited a Holling Type 3, or sigmoid, functional response, the search rate and handling time varying with both host instar and experimental environment. When provided with mixed-age host populations a marked preference was shown for the earlier instars. Results indicated that levels of superparasitism were negligible.
A high level of aggregation by parasitoids in areas where hosts are plentiful, resulting in non-random patterns of parasitism, promotes population stability. Trybliographa rapae's response to a hetero- geneous host environment and the resulting patterns of parasitism were explored, as were the effects of parasitoid density and host distribu- tion. In the laboratory, the parasitoid showed a strong tendency to aggregate on high host density patches. However, at high parasitoid densities marked dispersion away from these areas was observed. Similar patterns were observed in the field although the overall levels of para- sitism were considerably lower.
By placing cohorts of various numbers of different development stages of the cabbage root fly in the field the effects of six mortality factors were investigated. Egg predation, mainly by carabid and staphylinid beetles, appeared to be the most important regulatory factor, parasitism making only a minor contribution to the pest's regulation.
Finally, the use of laboratory experiments in the development of models describing host-parasitoid interactions and their application to natural situations has been considered in the light of these results. ACKNOWLEDGEMENTS
I am deeply indebted to many people for their help in this work. Foremost among these is my supervisor, Prof. M. P. Hassell, who has given constant guidance and encouragement throughout the duration of this study and has taught me much about the dynamics of insect populations. Sincere thanks are also due to Dr. P. M. Reader. As well as providing a helping hand whenever it was needed, Dr. Reader has always been available for discussion of various aspects of the work and I gratefully acknowledge her friendship, patience and un- failing humour. Drs. J. K. Waage and M. J. Crawley have given
readily of their time to advise me, particularly during the early stages of this study. I also acknowledge the understanding shown by my present supervisor, Dr. S. Finch, while this work was being completed.
My thanks are also due to Prof. M. J. Way and Prof. Hassell for making the research facilities at Silwood Park available and to the Natural Environment Research Council for the award of a research studentship. I am very grateful of the comradeship afforded to me by members of the Insect Ecology Group at Silwood Park, Nimmi Pallewatta and my laboratory colleagues, Emma Berkeley, Chien-Chung Cheng and Carlos Garcia, deserve special mention. Various people have provided me with advice, unpublished information and culture material: Drs. B. Bromand, R. H. Collier, W. J. Turnock and L. E. M. Vet, Julian Cottrell and Sharon Citrone. My sister, Bethan, has been a source of constant support and had the dubious pleasure of reading the final versions of this work. The thesis was typed by Mrs. D. Boyle.
Finally, I wish to thank my parents. Without their continual encouragement, support and devotion over the years this study would not have been possible and it is as a token of my appreciation that I dedicate this work to them.
Diolch o galon i chwi gyd! TABLE OF CONTENTS Page
Abstract 2
Acknowledgements 3
Table of Contents 4
List of Figures 7
List of Tables 10
Chapter 1 Introduction 12
Chapter 2 The Biology of Host and Parasitoid 18 2.1 Delia radicum (L.) 18 2.1.1 Biology of Delia radicum 18 2.1.2 Rearing of Delia radicum in the laboratory 21 2.1.3 Natural enemies of Delia radicum 23 2.2 Trybliographa rapae (Westw.) 24 2.2.1 Biology of Trybliographa rapae 24 2.2.2 Culturing of Trybliographa rapae 28 2.3 Life-history studies of Trybliographa rapae 31 2.3.1 Materials and methods 31 2.3.2 Results and discussion 32 2.4 Behaviour of Trybliographa rapae 40 2.5 Host location by Trybliographa rapae 43 2.5.1 Materials and methods 47 2.5.2 Discussion of experimental results 51 2.6 Aleochara bilineata (Gyll.) 59 2.6.1 Life-history of Aleochara bilineata 59 2.6.2 Culturing of Aleochara bilineata 61
Chapter 3 Host density and its effect on levels of parasitoid by Trybliographarapae 62 3.1 Functional Responses 62 3.1.1 Type 1 Functional Response 63 3.1.2 Type 2 Functional Response 66 3.1.3 Type 3 Functional Response 69 3.1.4 Estimating parameter values 71 3.1.5 Variation with experimental design 72 3.1.6 Population models and stability 75 5 Page 3.2 Experiment to determine the functional response of Trybliographa rapae in the presence of different host instars and on different plant substrates. 77 3.2.1 Materials and methods 77 3.2.2 Results 81 3.2.3 Discussion 88 3.3 Inter-Age-Class Preference 92 3.3.1 Detecting preference 92 3.3.2 Experiment to determine the searching preference of Trybliographa rapae for different developmental stages of its host, Delia radicum. 95 3.4 Superparasitism 104 3.4.1 Materials and methods 106 3.4.2 Results 108 3.4.3 Discussion 108 3.5 Multiparasitism 109 3.5.1 Materials and methods 110 3.5.2 Results and discussion 110 3.6 Conclusions 117
Chapter 4 The effects of host heterogeneity and parasitokl density on patterns of parasitism 119 4.1 Introduction 120 4.1.1 Host heterogeneity 120 4.1.2 Parasitoid density 126 4.2 Experiment 4.1: To determine the effect of a heterogeneous host environment on the levels of parasitism reached by a single niyblio- grapha rapae female. 131 4.2.1 Materials and methods 131 4.2.2 Results and discussion 133 4.3 Experiment 4.2: To determine the effect of parasitoid density on the pattern of para- sitism of Delia radicum by Trybliographa rapae. 144 4.3.1 Materials and methods 144 4.3.2 Results and discussion 144 4.4 Experiment 4.3: To determine the effect of host distribution on the levels of parasitism of Delia radicum by Trybliographa rapae. 158 4.4.1 Materials and methods 159 4.4.2 Results and discussion 160
4.5 General discussion 171 Page Chapter 5 Patterns of parasitism by Trybliographa rapae under field conditions 178 5.1 Introduction 178 5.2 Experiment 5.1: To determine the effect of host heterogeneity on the levels of para- sitism by Trybliographa rapae under field conditions. 181
5.2.1 Materials and methods 181
5.2.2 Results and discussion 183 5.3 Experiment 5.2: To determine the levels of parasitism by naturally occurring parasitoid populations on manipulated host densities. 192
5.3.1 Materials and methods 192
5.3.2 Results and discussion 192 5.4 Experiment 5.3: To determine the patterns of parasitism within a naturally occurring population of the cabbage root fly and its parasitoid Trybliographa rapae. 200
5.4.1 Materials and methods 201
5.4.2 Results and discussion 204
5.5 General discussion 213
Chapter 6 Mortalities affecting cabbage root fly populations 217 6.1 Introduction 217 6.2 A study to determine the effect of spatial heterogeneity on mortality factors affect- ing cabbage root fly populations in the field. 223 6.2.1 Materials and methods 223 6.2.2 Results 227 6.2.3 Discussion 245
Chapter 7 General discussion and conclusions 251
Bibliography 266
Appendices: Appendix 1 The natural enemies of Delia radiczon 293 Appendix 2 Synonyms of Trybliographa rczpae (Westw.) 297 Appendix 3 Derivation of the no-switch model 300 Appendix 4 Experimental results 303
LIST OF FIGURES
Figure Page
2.1 Development stages of Trybliographa rapae. 25
2.2 Emergence curves of host and parasitoid. 33
2.3 Relationship between parasitoid head width and hind tibia. 34
2.4 Relationship between parasitoid size and longevity. 34
2.5 Relationship between female parasitoid size and two measure of fecundity. 35
2.6 Oviposition record of Trybliographa rapae females. 37
2.7 Parasitoid survivorship curves. 39
2.8 Stages in successful parasitism. 44
2.9 Choice-chamber. 48
2.10 Apparatus used for testing the response of Trybliographa rapae to various chemical stimuli. 50
2.11 Graphical representation of data given in Table 2.8. 55
2.12 Path taken by parasitoid while foraging. 57
3.1 The functional responses described by Rolling (1959a.). 64
3.2 Experimental arenas. 80
3.3 Functional responses obtained in Experiment 1. 82
3.4 Functional responses obtained in Experiment 2. 84
3.5 Simulated relationships between the search rate 87 and host density.
3.6 Parasitism of Delia radicum by Trybliographa rapae when presented with two hosts. 97
3.7 Preference in parasitism when two hosts presented together. 100
- 8 -
Figure Page
3.8 Multiparasitism of Delia radicum pupae. 113
4.1 Hypothetical relationships between the time spent by a parasitoid in a patch and the host density per patch. 122
4.2 Over-aggregation curve. 125
4.3 Experimental arenas. 132
4.4 Patch-time allocation by a single foraging
parasitoid. 134
4.5 Patch-time allocation of a single female parasitoid at hourly intervals. 138
4.6 Times of successive visits. 140
4.7 Ratio of second to first visit on an individual patch. 142
4.8 Aggregative response of Trybliographa rapae. 145
4.9 The relationship between searching efficiency and parasitoid density. 147
4.10 Interference analysis. 150
4.11 The relationship between the time spent on host areas and parasitoid density. 151
4.12 The effect of parasitoid density on the allocation of searching time. 154
4.13 Total number of hosts parasitised under conditions of aggregated and even distributions. 161
4.14 Allocation of searching time on patches of equal host densities. 163
4.15 Interference analysis. 164
4.16 Superparasitism and interference. 170
5.1 Experimental arena used in Experiment 5.1. 182
5.2 Patterns of parasitism in laboratory and field. 184
9
Figure Page
5.3 Total number of host larvae parasitised in laboratory and field. 186
5.4 Searching efficiency in laboratory and field. 190
5.5 Interference in laboratory and field. 191
5.6 Predation as a factor of cabbage root fly larval mortality. 194
5.7 Parasitism of Delia radicum larvae by nTbliographa rapae. 197
5.8 Density dependent patterns of parasitism in the field. 198
5.9 Cabbage root fly distribution around a swede plant. 202
5.10 Cabbage root fly spatial distribution patterns. 205
5.11 Overwintering patterns of parasitism. 209
6.1 Egg mortality, 1984. 225
6.2 Density dependent relationships for larval mortality from predation. 228
6.3 Larval predation. 230
6.4 Larval parasitism. 232
6.5 Density independent pupal predation. 235
6.6 Patterns of pupal parasitism. 237
6.7 Mortality of cabbage root fly, 1983. 240
6.8 Mortality of cabbage root fly, 1984. 242
- 10 -
LIST OF TABLES
Table Page
2.1 Sex of emerging parasitoids from samples of overwintering pupae, 1982 - 1984. 27
2.2 Weights of healthy and parasitised Delia radicum larvae. 30
2.3 Development time of healthy and parasitised Delia radicum larvae. 30
2.4 Egg load dissections. 38
2.5 Light preferences of female parasitoids. 41
2.6 The effect of light conditions on parasitoid oviposition. 41
2.7 Preference of Trybliographa rapae females for
various chemical stimuli. 49
2.8 Chemical-induced changes in parasitoid locomotory behaviour. 52
2.9 Chemical-induced changes in parasitoid speed. 53
3.1 Parasitoid oviposition as affected by experience. 78
3.2 Parameter estimates for functional responses using Hassell, Lawton and Beddington's Type 3 model. 86
3.3 Parameter estimates for functional responses using a special case of Hassell, Lawton and Beddington's Type 3 model. 89
3.4 Statistical analysis of preference. 99
3.5 Superparasitism by Trybliographa rapae. 107
3.6 Multiparasitism of Delia radicum pupae. 111 - 11 -
Table Page
3.7 Weights of pupae parasitised by Aleochara bilineata. 111
3.8 Multiparasitism of Delia radicum pupae. 114
4.1 Patches visited on successive visits by a single female parasitoid. 135
4.2 Allocation of successive visits to five patches of various host densities. 136
4.3 Patch choice and experience. 139
4•4 Levels of superparasitism at various parasitoid densities. 157
4.5 Comparison of search rate under conditions of even and aggregated host distributions. 166
4.6 Comparison of total time spent foraging on patches under conditions of even and aggregated host distributions. 167
4.7 Comparison of the levels of superparasitism under conditions of even and aggregated host distributions. 169
5.1 Levels of superparasitism under both field and laboratory conditions. 187
5.2 Depth distribution of cabbage root fly pupae. 203
5.3 The number of pupae collected per swede plant, 1981 - 1984. 212
6.1 Experimental details of k-value study. 224 — 12—
CHAPTER 1
INTRODUCTION
The successful control of pest species by biological means has, over the last 10 - 20 years in particular, provided population ecologists with a forum for much debate. Both the structuring of a general strategy for biological control (for example, Huffaker and Messenger,1976) and
establishing the relevance of ecological theory to control programmes
(for example, Hasse11,1978) have emphasised various aspects of pest- natural enemy population dynamics. A number of workers are now generally agreed that successful biological control within a perennial crop arises by the natural enemy imposing a low, stable host equilibrium.
In developing such a theory most experimental work (see Hassell
(1978) for examples) has been carried out under laboratory conditions.
Thus, many of the vagaries of the field situation are eliminated and the consequences of interactions in population dynamic terms more easily classified. Population theory pertaining to biological control has, for
the most part, been derived from the Nicholson and Bailey (1935) model
(for example, Beddington, Free and Lawton,1978; May and Hasse11,1981;
Hasse11,1978,1980), a deterministic model describing the dynamics of a single host (or prey) species and a single parasitoid (or predator)
species. The more recent models have enriched the basic, earlier frame- work by incorporating more realistic parameters describing parasitoid behaviour.
As Hassell and May (1973) confirmed by a linearised stability analy-
sis, the Nicholson-Bailey model has an unstable equilibrium, yielding diverging oscillations when either host or paVtoid population is a, perturbed. Along with host specificity, synchrony of the paOitoid population with that of the host, a potential for rapid population - 13 - increase and a high searching efficiency, Hassell and May (1973) found that the aggregation of parasitoids in the more densely populated host areas led to a locally stable model. Free, Beddington and Lawton (1977) further showed that 'pseudo-interference' was another potential stabilis- ing mechanism. Pseudo-interference, arising from the differential exploitation of host-containing areas, was found to lead to decreased parasitoid efficiency as the parasitoid density increased. Numerous workers have subsequently considered parasitoid aggregation to be a major mechanism ensuring sufficient control (Hasse11,1978 and references therein) but as Hassell (1980) noted, the amount of aggregation may depend on host density and this complicates the relationship between aggregation and stability.
While Waage and Hassell (1982), in a review of recent developments contributing to the theoretical basis for the use of parasitoids in biological control, conclude that such a fundamental approach has a clear potential to control programmes of this kind, other workers have disagreed to varying extents.
Dempster (1975) for example, has argued that while such population theory has produced many fruitful ideas they are only of limited use in developing realistic population models and, he concludes, 'elaborate theories' explaining population regulation and stability should not be founded on such studies. That a low stable pest equilibrium plays a successful role in biological control programmes has also been recently challenged (Murdoch,1979; Murdoch, Reeve, Huf faker and Kennett,1984;
Murdoch, Chesson and Chesson,1985). The latter workers, in particular, suggest that even in persistent ecosystems local pest extinction, rather than stable pest equilibrium, may be a more appropriate goal for successful control. - 14 -
In the midst of such controversy it emerges that one of many un-
investigated fields of study is the relevance of laboratory studies,
on which a considerable amount of population theory is based, to the
field situation. The scarcity of comparable data from both field and
laboratory studies has made the establishment of any relationship difficult.
This study attempts to make such an investigation. By experimental mani-
pulation of both host and parasitoid populations, the level of searching
efficiency and aggregative response shown by a parasitoid in the labora-
tory are explored. Subsequently, by repeating a number of the laboratory
investigations in the field, in as natural an environment as experimental procedure will permit, comparisons are made between laboratory and field studies and an attempt made to establish the relevance of laboratory observations to what happens under natural conditions.
To carry out such an investigation it is essential to use a host- parasitoid system that enables both laboratory and field studies to be made with relative ease. The interaction between the parasitoid
Trybliographa rapae (Westw.) (Hymenoptera:Cynipidae) and the cabbage root fly, Delia radicum (L.) (Diptera:Anthomyiidae), provides such a system.
The abundance of natural populations in cruciferous crops and the relative ease with which laboratory cultures may be established and maintained provides an almost unique opportunity to study levels and patterns of parasitism under both conditions.
A knowledge of the basic life-history strategies of both host and parasitoid are essential for the full understanding of any such inter- action. The basic biology of the cabbage root fly is well known (for example, Coaker and Finch,1971). Relatively little is known of its main hymenopteran parasitoid, T.rapae, and in Chapter 2 the available literature is reviewed and some basic aspects of the wasp's biology
(for example, longevity and fecundity) are investigated. Another aspect - 15 -
of considerable importance in the control of pest insects is the means by which patitoids locate and select their hosts (Vinson,1981;1984a.).
While a detailed study of this behavioural aspect is beyond the scope
of the present study, it was considered important to gain some insight as to whether T.rapae exhibited any marked behavioural patterns to some of the various olfactory stimuli encountered within a cruciferous crop.
The results of some simple observations are discussed in Chapter 2.
The functional response of Solomon (1949) is the classical method
of investigating how a parasitoid responds to changes in the density of
its host. The various forms of this response, as described by Holling
(1959a.), are discussed in Chapter 3, as is more recent work that has
shown that such responses may not be as straightforward and uniform as
first believed. It has been shown that factors such as the developmental
stages of the interacting species (for example, Thompson,1975), experi- mental time (for example, Hofsvang and Hagver,1983) and plant structure
(for example, Carter, Sutherland and Dixon,1984) all play important roles
in determining the form of the functional response observed. In this
study the form of the response shown by T.rapae is investigated under
controlled environment conditions using the three developmental instars
of the host, D.radicum, and also on differing plant tissue structures.
Under natural conditions a host-parasitoid system is characterised
by each parasitoid individual encountering a range of host developmental
stages. The wasp may exhibit a preference for a particular host type
or may switch from one host category to another as relative abundances
change. In the latter section of Chapter 3 an attempt is made to explore
whether such behaviour is characteristic of the D.radicum - T.rapae
interaction, and experimental results are compared to those predicted by
the development of a model from the individual functional responses.
Finally, both superparasitism and multiparasitism are considered briefly - 16- and attempts made to determine the degree of discrimination against hosts previously parasitised either by a conspecific or by a staphylinid parasitoid.
The presence of heterogeneous environments in which certain areas contain more resources than others results in parasitoids showing aggre- gative behaviour in those regions that contain a high proportion of the host population (see earlier examples). As well as the pseudo-interference
arising from this aggregation, such behaviour may, in the presence of more
than one parasitoid, result in an increase in the rate of encounter between
individual parasitoids (behavioural interference). This may lead to an
increased tendency to disperse and a subsequent increase in the degree of
exploitation of the low density host patches. This is investigated in
Chapter 4. Various parasitoid densities are placed within a laboratory
arena where hosts are distributed either in a heterogeneous or homogeneous
pattern. As well as the level of parasitism recorded for different
patches, the patch-time allocation of the female parasitoids is also
analysed. Thus, patterns of parasitism may be related to the behavioural
responses of the foraging parasitoid population.
One of the major aims of this study is to relate the observations
made under laboratory conditions (Chapter 4) to those collected in the
field. This is considered in Chapter 5. Experiments where either host
or parasitoid populations are manipulated demand the use of an enclosed
environment and, as such, impose certain un-natural factors on the
observations made. However, by using a series of experiments which
progress from an enclosed field experiment to sampling from a cruciferous
crop, data are collected from which conclusions relating the various
experimental methods are then drawn. - 17 -
Chapter 6 is concerned with the relative contribution to the popula- tion dynamics of the cabbage root fly of various mortality factors operating spatially from plant to plant. The major causes of mortality affecting cabbage root fly populations are assumed to include predation of various developmental stages by carabid and staphylinid beetles, parasitism by T.rapae and Aleochara bilineata (Gyn.), a staphylinid parasitoid, and natural mortality within various instars. Although not a comprehensive study, an attempt is made to quantify the relative contri- butions of these various mortalities on a cabbage root fly population and to assess the importance of spatial density dependence within these factors.
The concluding discussion attempts to relate the various observations made during the experiments described above and to explain the observed patterns of parasitism by T.rapae on the basis of what has been learnt of the parasitoid's foraging behaviour. The use of laboratory experiments in the development of models describing host-parasitoid interactions and their application to natural situations is also discussed in the light of the study's results. - 18 -
CHAPTER 2
THE BIOLOGY OF HOST AND PARASITOID
The interaction between the cabbage root fly, Delia radicum, and
Trybliographa rapae is, as mentioned in the previous Chapter, in many
ways an ideal host-parasitoid system to study as it enables both
laboratory and field studies to be carried out with relative ease.
Natural populations occur in abundance in untreated (i.e. insecticide-
free) cruciferous crops making sampling and field experiments possible, while the establishment and maintenance of laboratory cultures allow
detailed laboratory studies to be made of the interaction throughout
the year.
2.1 Delia radicum (L.)
2.1.1 Biology of Delia nadicum.
Known as the cabbage root fly in Britain (Anon,1947) and the
cabbage maggot in North America (Muesebeck,1942), Delia radicum is
restricted to the temperate zone of the holarctic region (de Wilde,
1947a.; Commonwealth Institute of Entomology,1983). It is a destructive
pest of cruciferous crops in Europe and North America (Ministry of
Agriculture, Fisheries and Food (M.A.F.F.),1984), being most prevalent
on cabbages (Brassica oleracea var. capitata (L.)) and cauliflowers
(B.oleracea var. botrytis (L.)), although also damaging Brussels sprouts
(B.oleracea var. gemmiftra (Zenker)), radishes (Raphanus sativus (L.)),
turnips (B.rapa (L.)), swedes ( g .napus var. napobrassica (L.)) and many
cruciferous weeds (Schoene,1916; Brittain,1927; Smith,1927a.; Nair,
McEwen and Alex,1974; Finch and Ackley,1977). First described as
Anthomyia brassicae (Bouch6,1833), this name has now been superseded by
Delia radicum (L.) (Pont,1981) although other synonyms are frequently
encountered (Coaker and Finch,1971). - 19 -
The number of generations of cabbage root fly in a year depends on the prevailing climatic conditions. In general, the cabbage root fly has two generations each year in the north of the British Isles and three in the south (Smith,1927a.). Smith refers to these as the first, second and third generations, using 'generation' to describe the cycle starting at the adult stage and ending with the pupa. Miles (1954) and Hughes and Salter (1959) use 'generation' to describe the cycle starting from egg and ending with the adult, referring to the three generations as overwintering, first and second generations. In this study the definition of Smith, the most frequently used in Britain, is adhered to.
Adults of the first generation emerge from the overwintering pupae in late April and early May and, after a pre-oviposition period of
6 - 8 days, the females lay their eggs in soil crevices around the root of the host plant (Hughes and Salter,1959). The first eggs to appear
in the field coincide with the opening of the first flowers of cow parsley, Anthriscus sylvestris ((L.) Hoffm.) (Angiospermae:Umbelliferae),
in Southern England (Coaker and Wright,1963), while they are laid
slightly later, about mid-May, in northern areas of Britain (M.A.F.F.,
1984).
Under field conditions the eggs hatch within a week and the larvae move to the plant roots to feed. At the end of a 3 - 4 week larval
feeding period third instar larvae move away from the roots to pupate
in the soil. The next generation of adults emerge from the puparia within 2 weeks, provided there has been no induction of pupal aestiva-
tion (Missonier,1960; 1963) or diapause (Hughes and Salter,1959; Zabirov,
1961). The second generation of flies usually appears in late June and
July and the third generation from about mid-August onwards (M.A.F.F.,
1984). - 20 -
In southern areas of Britain, the late developing pupae from the
second generation and all pupae from the third generation enter diapause
when the third larval instar is subjected to changes in day length
operating through the host plant, or by temperatures below 15°C
(Hughes,1960; Missonier,1960; Soni,1976). The time interval needed
for completion of diapause has been used by Collier and Finch (1983,1985)
as a means of accurately forecasting the time of spring attack by the
first generation of fly populations.
Traynier (1967) found that more cabbage root flies were caught in
traps containing Brassica juices than in traps containing only water,
and suggested that odours help the fly to recognise its host plant.
Coaker and Smith (1968) found that the activity of gravid females
increased in the presence of chemicals that were possible constituents
of host plants, whereas odours from non-host plants had little effect.
Using a flight chamber they were also able to show that mated gravid
females would fly upwind towards sources of odour of either crushed
swede leaf or allylamine (a hydrolysis product of sinigrin, a charac-
teristic thioglucoside of Cruciferae). However, before landing on a host plant a suitable visual stimulus was required.
Preference for certain oviposition sites by the cabbage root fly has been positively correlated with the total thioglucoside present in varieties of B.napus (Coaker,1969). Doane and Chapman (1962) found that turnips were more preferred by the fly as oviposition sites than cauliflowers which are, in turn, more heavily attacked than cabbage
(Whitcomb,1945). Hardman and Ellis (1978) record work done at the
National Vegetable Research Station (N.V.R.S.) at Wellesbourne, Warwick showing the general order of increasing susceptibility to cabbage root fly to be Brussels sprouts, cabbage, cauliflower and radish respectively. - 21 -
Prior to oviposition D.radicum requires the presence of a contact
chemostimulus (de Wilde,1947a.). Coaker and Finch (1967) found that
solutions of sinigrin and allylisothiocyanate stimulated flies to
oviposit.
Using a mathematical model Hawkes (1968) estimated that flies
released into a Brassica plot dispersed at a rate of about 20 metres
per day. Coaker and Finch (1971) subsequently commented that at such
a rate populations in Brassica crops more than 800 metres apart would
be unlikely to intermix during the average field longevity of 2 - 3
weeks. This supported earlier work by Mowat and Coaker (1968) who
showed that the cabbage root fly had little innate tendency to disperse.
Finch and Skinner (1975) on the other hand, using females during the
first seven days of their adult lives, found that the dispersal rate
of the cabbage root fly was probably within a 2000 - 3000 metre radius
of the site of infestation. They argued that the estimates from earlier
work (for example, Hawkes,1968; 1972) could be solely a measure of the
dispersal due to the 'appetitive' flight (one which can be interrupted by stimuli which cause the insects to feed or lay eggs (Thorpe,1951))
rather than the 'migratory' flight (one which is relatively unaffected by stimuli (Southwood,1962; Corbet,1962)). Migratory flights commonly occur when insects are young and before their gonads are fully mature.
Hawkes (1968) used females 6 - 7 days old, wild populations being normally mature and ready to lay eggs when 5 - 6 days old.
2.1.2 Rearing of Delia radicum in the laboratory.
The method used for the continual rearing of the cabbage root fly was based on that described by Finch and Coaker (1969). To prevent induction of diapause, all stages of the life-cycle were permanently subjected to simulated summer conditions. The culture room was - 22- maintained at a temperature of 20 -I: 2°C and at a relative humidity of
70 ± 5 per cent. The oviposition cages (20 cm x 20 cm x 30 cm), constructed of metal frames covered by Terylene netting, were illuminated on a 16/8 hour light/dark cycle by fluorescent tubes suspended above the cages.
Adult flies were provided with nutrient in two petri dishes, one containing 10 per cent sucrose solution absorbed on a piece of cotton wool, the other a mixture of powdered brewer's yeast and yeast hydrolysate. Finch and Coaker (1969) found this arrangement to give the highest fecundity levels, giving an average longevity of 45 days and an average fecundity of 376 eggs per female. A water supply was also provided.
An oviposition site in the form of a swede cube set in a shallow dish of sand was positioned in each cage, the site being renewed every two days. On removal from the cages the eggs and sand were washed into a pot containing a swede root placed in wet sand. Since at relative humidities of less than 90 per cent the egg hatch becomes severely reduced (Finch and Coaker,1969), the eggs were covered with approximately 2 cm of wet sand and given a good watering. Watering only at time of egg inoculation and not at intervals throughout larval development resulted in larger pupae being produced, and the rotting of host plants became less of a problem. Leaf growth on swedes was removed to prevent colonisation by aphids and 'sticky' paper was interspersed between the pots to catch Drosophila adults and fungus gnats (Diptera:Mycetophilidae) which often emerged from the swedes.
Pupae were retrieved by flotation on water (Coaker and Finch,
1971) 4 - 5 weeks after inoculation and transferred onto moist - 23- vermiculite. The flies emerged within a further 10 - 20 days. Any pupae surplus to immediate requirements were stored in moist vermiculite at 3°C.
2.1.3 Natural enemies of Delia radicum.
Appendix 1 lists the natural enemies of the cabbage root fly
recorded in the literature. There are a large number of hymenopteran
parasitoids that attack the larval stages of the cabbage root fly, the cynipid Trybliographa rapae being the most abundant (Smith,1927a.;
Wishart, Colhoun and Monteith,1957). Parasitism of the pupae by species
of the genus Aleochara (Coleoptera:Staphylinidae) is common, A.bilineata
(Gyn.) usually being more common than A.bipustulata (L.) (Wishart,1957;
Coaker and Finch,1971). These two Aleochara species were found to
parasitise 20 - 30 per cent of the cabbage root fly pupae at N.V.R.S.,
Wellesbourne (Coaker,1966) and occasionally levels of up to 60 per cent
have been recorded in Canada (Wishart,1957). The fungus EMpusa muscae
(Cohn) (Eumycota:Zygomycetes) kills adult cabbage root flies while
Strongwellsea castrans (Batko and Weiser) (Eumycota:Zygomycetes) only
sterilises them (Smith,1927b.; Batko and Weiser,1965).
The immature stages of the cabbage root fly are also food for many
arthropods. Eggs are preyed on by trombidiid mites (Gibson and Treherne,
1916), ants (Schoene,1916) and carabid and staphylinid beetles (Wishart,
Doane and Maybee,1956), while larvae fall prey to ants (Schoene,1916),
beetles (Abu Yaman,1960) and other anthomyiid larvae (Smith,1927a.).
Although Coaker and Finch (1971) report that there are probably many
predators of the adult stage only a few anthomyiids (Schoene,1916) and
scathophagids (cordylurids) (Hobby,1931; Read,1958) have been recorded.
Read (1958) noted that Scathophaga stercoraria (L.) (Diptera:
Scathophagidae, but classified as Anthomyiidae by Read (1958)) stalks - 24 - and attacks its prey at rest, grasps it firmly between its forelegs and pierces the cervical region with its mouthparts. It can apparently feed on one fly for as long as 25 minutes, ingesting all the non-sclerotised contents of the body.
2.2 Trybliographa rapae (Westw.)
2.2.1 Biology of Trybliographa rapae.
The parasitoid T.rapae was first recorded associated with Brassicas
by Farmer (1835) who believed it to be the cause of 'fingers and toes'
or clubroot, Plasmodiorphora brassicae (Woron.) (Myxomycota:
Plasmidiophoromycetes). Westwood (1835), in commenting on this record,
identified the wasp as the cynipid Eucoila rapae. The nomenclature of
T.rapae is very difficult with at least 9 synonyms and another 9
possible synonyms. Appendix 2 lists the names believed to be synonymous
with T.rapae, the most frequently encountered in the literature being
Idiomorpha rapae (Westw.) and Cothonaspis rapae (Westw.).
Except for Japan, T.rapae is a cosmopolitan parasitoid being found
world-wide wherever the host insects are abundant (Wishart and Monteith,
1954). The cynipid, as well as being a parasitoid of D.radicum, also
attacks other anthomyiids, namely the bean seed fly, D.platura (Meig.),
the turnip root fly, D.floratis (Fall.), and the onion fly, D.antiqua
(Meig.) (Hamanond,1924; Lundblad,1933; de Wilde,1947b.; Wishart and
Monteith,1954). Wishart and Monteith (1954) found that attack by
T.rapae in the samples they examined varied from 1 to 45 per cent of
the total host population.
Having encountered a host and found it suitable for oviposition
the female wasp lays an egg by means of a long ovipositor which
penetrates the host larval skin. The egg of T.rapae is similar to that A
0•1mm
11•n••nIa 0.1mm
0•5mm
0•5mm
Figure 2.1 Trybliographa rapae (Westw.). A - Ovarian egg;
B - Egg one hour after oviposition;
C - Newly hatched larva; D - Fourth instar larva;
E - Pupa. (from Moltschanova,1930). - 26-
of other parasitic Cynipidae (Richards and Davies,1977). It is ovoid
in shape when newly laid with a long stalk or pedicel (Figure 2.1, A.
and B.). The function of the pedicel is uncertain; tube-like in form
and bearing the micropyle at its tip, the anterior end, it is thought
likely that it plays some role in the egg's movement down the ovipositor
(Chrysta1,1930). In certain hymenopteran species, for example members
of the genus nastothrix (Hymenoptera:Encyrtidae), the pedicel protrudes
through the body wall of the host and functions as a kind of respiratory
funnel enabling newly hatched larvae to breathe outside air (Imms,1918).
From oviposition to hatching requires some 96 hours at 20°C and
the emerging larva remains in its first instar until the host puparium is
formed. A host attacked early in its first instar results in the parasitoid's first instar being of longer duration than when the host is attacked in the late second or early third instar stage.
Hyper-metamorphosis (a type of parasitic insect life cycle involv- ing transformation through at least two distinctly different larval types) occurs in the larvae of all the entomophagous Cynipidae that have been studied (Wishart and Monteith,1954). The first instar larva is eucoiliform (Figure 2.1C.), having a distinct head, thoracic segments bearing fleshy, leg-like appendages and a long caudal appendage. The second instar of the parasitoid develops on pupation of the host. This instar is more cylindrical in shape and has considerably reduced appendages. The third instar is slightly flattened dorso-ventrally.
Both second and third instars are of relatively short duration lasting no more than five or six days at 20°C. Once the pupal characters are assumed by the host inside the puparium, development of the parasitoid is rapid. The parasitoid leaves the host pupa shortly after the forma- tion of the third instar by gnawing a hole near the head region. It takes up a position facing forward and feeds at the hole from which it Number of Number of Trybliographa rapae Year pupae Total Male Female
1982 A. 143 34 18 16
1982 B. 175 85 43 42
1983 222 58 33 25
1984 288 117 62 55
Table 2.1 Numbers of male and female Trybliographa rapae
emerging from samples of overwintering pupae
taken at Silwood Park, Ascot during 1982 - 1984. - 28 - made its exit. The external feeding stage of the third instar larva lasts one or two days. After the fourth instar larva, a typical, grub- like hymenopteran larva (Figure 2.1D.) is formed, feeding continues until all that remains of the host pupa is cuticula. A few days after feeding
is finished the meconium is voided and appears as dark, irregular blotches in the posterior end of the host puparium. The fourth stage may last about two weeks to several months, depending on temperature and other environmental factors. No cocoon is formed, the pupal (Figure 2.1E.) period lasting approximately one week. On emergence the adult gnaws an
irregular hole in the puparium, the earliest emergents being largely males. Trybliographa rapae overwinters as a fourth stage larva in the host's puparium.
Trybliographa rapae exhibits haploid facultative arrhenotoky where
females lay fertilised (diploid) eggs which give rise to females, and unfertilised (haploid) eggs which develop parthenogenetically into males.
There was no significant deviation (e-test, p >> 0.05, 1 d.f.) from a
50:50 male:female sex ratio; samples of overwintering pupae from Silwood
Park, Ascot yielded 53, 51, 57 and 56 per cent males in 1982 (A. and B.),
1983 and 1984 respectively (Table 2.1). Laboratory cultures yielded
similar ratios.
2.2.2 Culturing of Trybliographa rapae.
The parasitoid was maintained in culture, under the same environ-
mental conditions as the cabbage root fly, using a method described by
B.Bromand (pers.comm.), in which between 30 and 60 per cent of the
larvae provided as potential hosts were parasitised. Eggs of D.radicum
were washed onto a swede slice whose surface had been lightly scored
with a knife to aid the penetration of cabbage root fly larvae. This
was left for 7 days to ensure that the eggs had adequate time to hatch - 29 -
and the larvae to burrow into the swede slice. The slice of swede was
then placed on damp vermiculite and positioned in a cage containing
T.rapae females. The cynipids were left to parasitise the cabbage
root fly larvae for 7 days, then the swede slice was removed and
placed on vermiculite in another plastic sandwich box. When fully
grown the larvae moved out of the swede tissue into the surrounding
vermiculite to pupate.
The cynipids were provided with a 10 per cent sucrose solution
absorbed on cotton wool and a small quantity of yeast extract. Since
certain parasitoids such as Itoplectis conquisitor (Say) (Hymenoptera:
Ichneumonidae) show higher levels of fecundity when allowed to feed on
pollen constituents (Leius,1961), a pollen mixture was also provided.
This, however, had no influence on levels of parasitism and the wasps
showed little interest in the pollen's presence.
It was found that healthy and parasitised individuals could be
classified on their pupal weights. Table 2.2 records these weights
and a significant difference was found to exist between the weight of
parasitised and unparasitised pupae. Wishart and Monteith (1954) found
a similar difference when pupal lengths and diameters were measured.
These measurements did, however, show considerably more variation than
those obtained from weighing. This reduction in size is either due to the parasitoid slowing the growth rate of the host larvae which pupate at the usual age or else is the result of parasitised larvae growing at the normal rate but pupating at an earlier age. James (1928) supports the latter, but observations in the present study suggest that there was no significant difference between the timing of pupation for both conditions (Table 2.3). Number in Pupal weight sample (g)
Unparasitised pupae 85 0.017 ± 0.001
Parasitised pupae 117 0.010 ± 0.001
Table 2.2 Mean weight ( ± 95 per cent confidence intervals)
of healthy and parasitised Delia radicum pupae
sampled from Silwood Park, Ascot in November 1982.
Values are significantly different (Student's
t-test, p < 0.001).
Number in Days until sample pupation
Unparasitised larvae 69 25.9 ± 1.0
Parasitised larvae 74 25.2 ± 0.8
Table 2.3 Mean time ( ± 95 percent confidence intervals)
between egg hatching and pupation for unparasitised
and parasitised Delia radicum larvae, (Student's
t-test, p > 0.1). -31 -
2.3 Life-history studies of Trybliographa rapae.
James (1928), Moltschanova (1930) and Wishart and Monteith (1954) have also considered aspects of the biology and abundance of T.rapae, the latter authors, in particular, providing detailed descriptions of the immature stages and the adult parasitoid's reproductive physiology.
To determine the emergence, ovipositing and survival patterns of the parasitoid, the following set of simple experiments were designed.
2.3.1 Materials and Methods.
Emergence patterns.
Females (1 day-old) were allowed to oviposit for 24 hours in
2 day-old cabbage root fly larvae feeding on a swede disc (diameter
35 mm, thickness 5 mm). The resulting pupae were collected and the date and sex of the emerging insects noted.
Ovipositing pattern.
Females (0 - 2 hours after emergence) were removed from culture and placed in glass tubes with males. Mating and copulation took
place readily. Single females were then placed in a 'butter' dish
(base diameter 9 cm, height 4 cm) with a swede disc on which 30
cabbage root fly larvae had been placed 24 hours previously. Humidity
was maintained in the dish by a moist filter paper, and a small ball
of cotton wool soaked in sugar solution was placed to provide a source
of nutrient for the wasp. The swede discs and larvae were replaced
every 48 hours. The larvae, having been exposed to the parasitoids,
were dissected and the number of eggs laid recorded. Immediately
after oviposition the eggs of the parasitoid are entirely hyaline and
are difficult to see. To minimise errors in egg counts the parasitised - 32 - host larvae were kept for about 24 hours at 20°C prior to dissection.
After this period the eggs were more opaque and easier to find. To dissect, an incision was made at the posterior end of the larva by the prominent posterior tubercules. The eggs were usually exuded free of the viscera but a thorough search was necessary as some eggs were located deeper within the tissue mass.
Longevity studies.
The survivorship of the female parasitoid in the presence of excess hosts was obtained from the results of the oviposition studies, as was the pattern shown by males under the same conditions. Survivor- ship curves were also obtained for females placed with non-infested swede discs, i.e. no hosts were made available.
2.3.2 Results and Discussion.
Trybliographa rapae individuals emerged approximately 9 days later than D.radicum which had a mean developmental period of 37.7 ± 1.9 days
(mean ± 95 per cent confidence intervals) (Figure 2.2). Such a sequence of emergence illustrates how well their life cycles are synchronised.
The nine day period allows sufficient time for the adult D.radicum to oviposit and for the eggs to hatch (4 - 7 days and 3 - 4 days respec- tively at 20°C (Finch and Collier,1984)) before females of T.rapae begin to search for the D.radicum larvae. Male T.rapae emerge approximately 45.5 days after the parasitoid egg is laid, while females take an extra 2 - 2.5 days to complete their development. The earlier emergence of males ensures that when the females emerge there are sufficient males present to mate with them. The males remain in the vicinity of the area of emergence until the females have appeared. 46 25 26 1.0— nP m 0
• • 0 0 • 0 0•13— te 0
o • er) 0.6— E 0 •
• D.radicum k 0.4— • • T.rapae males 0 T. rapae females
0.2— 010 • II .- • • 0 00. 7-5--- F 1 20 30 40 50 60 70 Days after egg laid.
Figure 2.2 Emergence curves for Delia radicum and Trybliographa
rapae (curves fitted by eye). Final numbers of
individuals emerging for each category are also
given. • 0.90- • 2 • •
-E- E 0.75- . 3 .c ..-----..-'---'---- 71;C o'9 2 •2 22. 0.60- to 3 ._:a • • • ...... t.,..../ 2 0.45- i •2
0.30—, I I r r i 0.30 0 . 40 0.50 0.60 0.70 0.80 Head capsule width (mm).
Figure 2.3 The relationship between head width and hind tibia
length in Trybliographa rapae. (Equation of line,
y = 0.45x 4- 0.35; p < 0.02).
24.0-
,7;20.0- • to .13 —16.0-c ID a. 2 l' 120- 0 .-a) ._ • ...... n-•2 0 80- • CD E e u. 4.0- •
0. 0 I 1 I I I 0. 3 0.4 0.5 0.6 0•7 0.8 Head capsule width (mm).
Figure 2.4 The relationship between adult female parasitoid
size (as measured by head width) and longevity.
(Equation of line, y = 25.06x - 0.05; p < 0.001). - 35 -
a.
90- •
.2 • • • 1-2 i-0 30- • .2
0.3 04 0.5 0.6 0.7 0.8 Head capsule width (mm).
b.
4.5-, .2
13 • • • • • .2• • .2 • .2
0•0 I I i 1 0.3 0•4 0•5 0.6 01 0.8 Head capsule width(mm).
Figure 2.5 The relationships between female parasitoid size
and two measures of fecundity, (a.) total number
of eggs laid (equation of line, y = 57.23x - 4.66;
p < 0.005), and (3.) the mean number of eggs laid
per day. - 36 -
Under the experimental conditions described above T.rapae females
laid, on average, 37.7 (± 5.9) eggs during their lifetime, with con-
siderable variation between females depending on life-span. Width of head capsule provided a relatively accurate index of body size, as measured by the length of the left hind tibia (Figure 2.3). Larger
sized individuals lived longer (Figure 2.4) and had a higher total
fecundity (Figure 2.5a.). However, there appeared to be no correlation
(r = 0.16, p > 0.1) between size of individual and mean daily fecundity
(Figure 2.5b.). This simplified considerably the standardisation procedure used for experimental parasitoids.
The oviposition record of females provided with excess second
instar hosts is given in Figure 2.6. During the first 4 to 6 days of their lives the females maintained a reasonably constant oviposition rate of approximately seven eggs per 48 hours. There was, subsequently, a general decrease in the number of eggs laid but there was considerable variation. The ability to lay eggs immediately after emergence agreed with the observation by Wishart and Monteith (1954) that dissection of freshly emerged females revealed the presence of large numbers of mature ova (i.e. T.rapae is pro-ovigenic). Sexual maturity at emergence has also been reported for other cynipids by Roberts (1935).
Females starved of hosts for up to 4 days showed no significant difference in the number of eggs laid per two day period, the oviposition pattern being moved forward by the appropriate period. Adult parasitoids starved of hosts for longer than this showed a decrease in the number of eggs laid per observation period, suggesting that starvation of potential hosts may have resulted in resorption of some of the mature egg mass.
Dissection of females starved of hosts for various periods revealed a
similar pattern (Table 2.4). Flanders (1942,1945) found that if a
synovigenic female parasitoid does not obtain proteinaceous food or is
1 0-
9-
8- 29 30
o 7- .c 29 6- c
1-
0 1 1 1 1 1 I 1 1 1 1 0 2 4 6 8 10 12 14 16 18 20 22 24 Days since emergence and mating.
Figure 2.6 The oviposition record of Trybliographa rapae females
provided with excess hosts. (Values are given as
mean ± 95 per cent confidence intervals with
number of females surviving at the end of each
48 hour period.) Days without Number eggs hosts subsequent counted in to emergence dissected ovarioles
0 73.8 ± 5.0
2 74.0 ± 5.9
4 72.4 ± 5.0
6 65.4 ± 6.4
8 64.6 ± 3.4
10 57.2 ± 6.5
15 51.6 ± 11.5
20 38.2 ± 7.1
Table 2.4 The mean number of eggs (± 95 per cent
confidence intervals) dissected from the
ovarioles of Trybliographa rapae females
starved of hosts for various periods after
emergence. 1 • 0 0-0.._. • • --o...... 6...... m T.rapae males • ONO\ • T.rapae females with hosts \ 08.- • 0 0 T.rapae females without hosts \ eit \ ._>C \ \ .->.. 06-. co= C \ o 0 z .. • • \\I\ 2 a. \• \ \ 0.2- s 0
\a \ Ili._...... 0-.... 0.0 [ 1 T 11 1 11F ...41i ", 9--r 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 Days after emergence.
Figure 2.7 Survivorship curves for Trybliographa rapae
showing the effect of host availability on
female longevity. (Initial number of parasitoids
in each case = 30). - 40 - unable to find hosts for an extended period of time, the ripe eggs in the ovarioles are absorbed. Whether this is common in pro-ovigenic insects is uncertain.
Trybliographa rapae males had a mean lifespan of 9.5 ± 1.2 days.
Females provided with excess hosts lived for 14.4 ± 1.8 days while
those provided with similar food sources, sucrose solution and swede,
but no hosts lived for 21.9 ± 2.3 days (Figure 2.7). As the females
were not observed to host feed to replenish their energy supplies, the
shorter life span of ovipositing females suggests that a considerable
amount of their energy reserves is apportioned to actual host location
and oviposition.
2.4 Behaviour of Trybliographa rapae.
In general, adult T.rapae are not very active, spending considerable
lengths of time resting and cleaning. They are not strong fliers, and
most active movement involves walking. When placed inside a container
partly covered with dark paper, no phototactic response was shown,
equal numbers of females spending their time in the artificially lit
area as did in the shaded region (Table 2.5). Levels of parasitism
under the two light regimes also showed no significant difference
(Table 2.6).
Copulation may occur immediately upon emergence from the host
puparia. The male mounts the female waving his antennae. If receptive,
the female raises her antennae, which are shorter in length than the
male's, and the two pairs of antennae are rubbed against one another.
When not receptive, the female places her antennae on the substrate in
front of her, and the male eventually dismounts. Copulation only
requires from 30 to 60 seconds. If hosts are available, oviposition
by mated or unmated females may take place within a few hours of
emergence. Number of Trybliographa rapae females
Light Dark
29 21
Table 2.5 The number of female parasitoids recovered
from shaded and open areas of arena.
(Data for 5 replicates pooled together;
2 for significant difference, p > 0.05,
1 degree of freedom.)
Number of eggs laid in 48 hour period
Light Dark
8.2 ± 1.8 7.6 ± 2.1
Table 2.6 The effect of light conditions on the oviposition
(mean for 5 females ± 95 per cent confidence
intervals) of one day-old Trybliographa rapae
females. (Student's t-test, p > 0.05, 8 degrees
of freedom). - 42 -
James (1928) reported that females would not oviposit in bright light, or without the pieces of plant containing the larvae being buried in the soil. As shown during the present study, females ovi- posited readily in the bright, artificial light of the laboratory.
However, difficulties were encountered in persuading the female to oviposit when larvae were presented without the host plant. The
parasitoid showed negligible interest when naked larvae were present, and very little when larvae were placed under moist filter paper.
Wishart and Monteith (1954) reported that larvae were quickly located by females in this latter situation. When larvae were presented in a
swede 'puree', parasitism occurred; the number of hosts parasitised was, however, significantly lower than when the larvae were burrowing
into a solid swede disc. It may be that oviposition behaviour was encouraged by the active probing of the Brassica substrate. Under
these conditions the host was not visible and observing an actual
oviposition difficult. Attempting to differentiate between normal probing behaviour and that when an oviposition was taking place proved both time consuming and very unrewarding.
Typically, T.rapae females make short walking periods on the
substrate surface and, on stopping, probe the surface intensively.
Probing does not occur while moving. The parasitoid makes regular use of its antennae by palpating the substrate continuously while moving. Such physical cues are know to operate for various para-
sitoid species over varying distances. Vet and van Alphen (1985)
report that in reaction to a source of movement on the surface of the
substrate, as with a small brush, female T.rapae often probed deeper
into the substrate rather than probe directly towards the source of movement. Soper, Shewell and Tyrrel (1976) found that Calcondamyia auditrix (Shewell) (Diptera:Sarcophagidae) responded to the sound
produced by the male cicada host, Okanagana rimosa (Say.) - 43 -
(Hemiptera:Cicadidae), over metre distances. In contrast, Biosteres
longicaudatus (Ashmead) (Hymenoptera:Braconidae) only responds to substrate vibration produced by the feeding activity of its host,
Anastrepha suspensa (Lowe) (Diptera:Tephritidae), over short distances
(Lawrence,1981). Laboratory observations showed T.rapae to have considerable searching abilities, penetrating up to 3 cm into the burrows made by the host larvae. The parasitoid's behaviour appears to be specialised towards searching for hosts that are present in the deeper layers of the substrate. This is not surprising as the majority of the larvae attacked by T.rapae, as well as being below the surface are also embedded in plant tissues.
2.5 Host location byTryb/iographarapae.
The location of a suitable host for oviposition has been considered to take the form of a sequence of responses involving several levels of stimulus. Salt (1935) and Laing (1937) divided the processes culminat- ing in successful parasitism into two steps: host habitat location followed by host location. Doutt (1959,1964) considered four such steps: host habitat location, host location, host acceptance and host suitability. Vinson (1975) has added host regulation, the ability of the parasitoid to alter its host for the benefit of its progeny, as a fifth step. More recently, Vinson (1984a.) has further subdivided the host selection process (the first three stages of Doutt) into seven sub-categories. These are summarised in Figure 2.8. Hassell and
Southwood (1978), in their review of the foraging strategies of insects, consider the forager as perceiving its environment at several hier- archical levels. These may be classified as the habitat where, in the case of parasitoids, potential hosts may be present, the patch where hosts actually exist, and then finally the resource itself, the actual host. Waage (1979) suggested this to be so in his study of the SUCCESSFUL PARASITISM
I I I HOST SELECTION HOST SUITABILITY
I I 1 1 1 1 HOST HOST HOST HOST FINDING ACCEPTANCE CONSTRAINTS REGULATION
----0—_—__1 f Habitat Host Preference Examination 1 1 Environmental Environmental t I Ovipositor Potential Probing I I Host Physiological Physiological Community t Location OvipositorDrilling I I I Competitive Behavioural Host Location I 1 Oviposition
Figure 2.8 Successful parasitism can be divided into four
sub—categories. The first two are concerned
with the selection of hosts, while the last
two are concerned with the suitability of the
host as an environment for the development of
the parasitoid's progeny. The arrows provide
an idea of the flow of the parasitoid through
the various steps. (taken from Vinson,1984a.) - 45 - ichneumonid parasitoid Venturia ( = Nemeritis) canescens (Grail.) where three levels of foraging could be determined - movement of the para- sitoid between patches of grain in granaries, between host (Plodia interpunctella (Hubn.) (Lepidoptera:Pyralidae)) patches in grain and between hosts in host patches.
The method by which foragers locate actual host patches can show considerable variation. It is common for parasitoids to be attracted to the food items of the host and, as a consequence, encounter the patch almost incidentally. Hubbard (1977) has shown that the mustard oils emanating from Crucifera play an important role in habitat location in Apanteles glomeratus (L.), a braconid parasitoid of the large cabbage white butterfly, Pieris brassicae (L.) (Lepidoptera:Pieridae). Similarly,
Read, Feeny and Root (1970) have illustrated the importance of these chemicals in the habitat selection of another braconid, Diaeretiella rapae (Curtis), a parasitoid of the cabbage aphid Brevicoryne brassicae
(L.) (Hemiptera:Aphididae). Nasonia vitripennis (Walker), a pteromalid parasitoid of many species of cyclorrhaphous pupae, is also known to be attracted to the odour of carrion irrespective of whether or not their hosts are present in the meat (Laing,1937). Bragg (1974) found that
Phaeogenes cynarae (Bragg) (Hymenopteradchneumonidae) was attracted to the host plant, further stimulated by the addition of plant juice and ultimately stimulated to attack by host (Platyptilia carduidactyla
(Riley) (Lepidoptera:Pterophoridae)) movement in the presence of the other two. Finally, Vet (1983) found that Leptopaina clavipes (Hartig)
(Hymenoptera:Eucoilidae) females show a response to the odour of decaying mushrooms in a state likely to contain their dipteran larval hosts, fungivorous Drosophila.
Waage (1978) suggests that at each level in the hierarchical sequence, two sorts of stimuli operate: 'attractant' stimuli which elicit orientation to areas containing hosts, and 'arrestant' stimuli - 46 -
(sensu. Dethier, Browne and Smith,1960) that elicit a slowing of the parasitoid's linear progression by reducing actual speed of locomotion or by increasing their turning rate. Once arrested in such areas, parasitoids may then respond to further attractant and arrestant stimuli which localise their movements to even smaller units of host distribution. Noyes (1974) provides such an example from the ichneumonid parasitoid Diadromus pulchellus (Wesm.) and its host, the leek moth
(Acrolepia assectella (Zeller) (Lepidoptera:Yponomeutidae)). At one level the ichneumonid is attracted to olfactory stimuli from the host's food plant, leeks. Once arrested on these, it forages at another level, exhibiting arrestment in areas of the plant containing a chemical produced by the host itself.
Using an airflow olfactometer L.Vet(pers.comm.) has observed that
T.rupae females are attracted by Brassica odours. It was found that a stronger response was obtained when the wasps were presented with broken turnip leaves as compared to whole leaves. Such evidence suggests that, on emerging from the host's puparium, a female T.rapae will locate the host habitat by following olfactory cues from the host plant. Finch
(1976) has shown that the host, the cabbage root fly, is also attracted over considerable distances by the mustard oil glucosides emanating from the Crucifera. The response may only be of importance for the first generation of parasitoid adults as the second generation will, in most cases, emerge within the habitat in which they are likely to find potential hosts.
Two short, simple, experimental studies were carried out to deter- mine the ability of T.rapae to differentiate between the various chemical stimuli present in an area of Brassicas and to explore the effect of olfactory stimuli on the behaviour of the wasp. As both were carried out in small laboratory arenas the actual mechanism of attraction of the wasp by any specific stimulus could not be established. - 47 -
2.5.1 Materials and Methods.
Experiment 1: To explore the olfactory behaviour of Trybliographa rapae
to various chemical stimuli.
This experiment was based on similar studies by Selander, Kailo,
Kangas and Perttunen (1974) and Murphy (1982), where wasps were presented with two different substrates in a choice-chamber olfactometer (Figure
2.9). The lower half of the chamber consisted of a platform on which
the two substrate containers were positioned. The swede was presented as small discs, as previously described. The upper half of the choice- chamber formed an arena with a hole in the centre of the upper surface
to enable parasitoids to be introduced. The floor of the arena was made of fine muslin so that the volatile chemical components from the treat- ments could permeate upwards into the appropriate side of the arena.
Humidity on each side of the arena was measured in a preliminary run with each treatment using cobalt thiocyanate paper. If found to be unequal, this was corrected by placing a dish of water next to the appropriate container.
Ten standardised females (mated and 24-28 hours old) were introduced
into the arena of the choice-chamber olfactometer and left for 12 hours.
The number of females on each side of the chamber was then recorded.
The procedure was repeated ten times, and the results obtained are
given in Table 2.7.
Experiment 2: To study the arrestment response of Trybliographa rapae
to chemical stimulus produced by its host, Delia radicum.
The experimental chamber used in this experiment is shown in
Figure 2.10. Females standardised as mentioned above were introduced
individually into the chamber and allowed to acclimatise for 30 minutes.
One of the five different substrates used was then placed in the centre Figure 2.9 Choice-chamber used to measure the ability of
Trybliographa rapae to differentiate chemical
stimuli likely to exist in a Brassica crop.
The diagram shows a cross section through the
chamber; A: hole to introduce experimental
wasps, B: arena, C and D: containers for
substrates. Substrate Number females 2 X A B A
Fresh Swede Blank 66 34 10.24**
8 day old Swede Blank 68 32 12.96***
Rotten Swede Blank 74 26 23.04***
8 day old infested Swede Rotten Swede 60 40 4.00*
8 day old infested Swede 8 day old Swede 61 39 4.84*
Table 2.7 The preference of Trybliographa rapae females for
various volatile chemicals emanating from different
areas of the choice-chamber (Figure 2.9).
(Data for 10 replicates pooled together; significant
difference shown by 0-test (1 degree of freedom) -
* indicates p < 0.05; ** - p < 0.01; *** - p < 0.001). a. cias=s3ascramm-1.=xxx3=
-= 7= 7= 1;.= "= .= = = A
AMIN
b.
Figure 2.10 Apparatus used for testing the response of
TrybZiographa rapae to various chemical stimuli
(a.) cross section of arena, A: substrate,
B: Terylene netting, C: glass plate on which
wasp's path was drawn, (D.) Terylene netting
(B) showing area of chemicals (D) emanating
from substrate. - 51 - of the lower compartment, still covered at this stage to prevent any chemostimulants penetrating into the experimental chamber. The cover was then removed and the wasp was observed for 15 minutes, its path being recorded on the glass surface used as a lid. The time spent on the patch while both moving and stationary was recorded, and the speed on both patch and non-patch areas estimated. Five runs were made daily, each treatment being used once per observational period. Ten wasps were used for each of the different substrates. The results are presented in Tables 2.8 and 2.9.
Significant differences between treatments were established using the F-test. To compare pairs of treatment means the advice of Carmer and Swanson (1973) was followed. They report that the least significant difference method is a very effective test for detecting true differences in means provided that the F-test in the analysis of variance is signifi- cant at 5 per cent.
2.5.2 Discussion of Experimental Results.
From Table 2.7 it would appear that T.rapae females showed a significant preference for areas having strong Brassica odours. This lends support to the suggestion that the location of the habitat of potential hosts by T.rapae may indeed be by an olfactory response to volatile chemicals emanating from the host plant. Examples have already been cited which illustrate that such chemostimulants are commonly used for host habitat location by numerous parasitoids. In particular,
Carton (1976) found that a closely related species to T.rapae of the genus Cothonaspis (Hymenoptera:Eucoilidae), which attacks larvae of
Drosophila melanogaster (Meig.) (Diptera:Drosophilidae), responded to ethanol from a distance. As the hosts are found in fermenting fruit it is likely that the chemical functions to orientate the female parasi- toids to an environment that may contain potential hosts.
• •
— 52 —
cel o 1/40 .0 -.7 0 0 0• 0• 0 0. 0 0 t) +I +I +4 4-1 +I L. co
n CN•I c •I 0 0
N. •n••• L. to 0 0 0
-H -H +I +I +I 4.0 N. NI CO • • • • 0- a a CNI C5C•11
. oo
CT N. r)C N. csi -4
-H -H +I +I +I a ....? a °3. . • • • %Jo cl, cs, -- cn 1/40 N. Crl
• • in 0 0 N1 co Cr) 40 •.0 a) 0 cl) +I +I +I +I +I co co ON Cr) ...7 . . . N. .— CT N. -4 n.10 ....+ %.0 •—• .—
Speed on Speed off Student's
Substrate patch area patch area t-test
(cm. sec.) (cm. sec.-1)
Moist filter paper 0.41 ± 0.03 0.42 ± 0.07 0.20
Washed 3-day old larvae 0.43 ± 0.06 0.43 ± 0.07 0.07
Unwashed 3-day old larvae 0.25 ± 0.06 0.50 ± 0.14 3.77***
3-day old Swede disc 0.24 ± 0.06 0.40 ± 0.08 3.76***
3-day old Swede disc with larvae 0.26 ± 0.04 0.50 ± 0.13 3.98***
Table 2.9 The speed of movement of female Trybliographa rapae
inside and outside areas (patches) of chemostimuli
from different substrates. (Results are given as
mean ± 95 per cent confidence intervals for 10
wasps; *** indicates p values < 0.001). - 54 -
When non-infested swede was placed with infested swede a significant preference was shown for the infested disc. The ability to discriminate between infested and non-infested Brassicas is of considerable importance for the parasitoid's energy conservation and can arise from one or a combination of factors. The presence of larvae may, in itself, be a direct stimulus. However, the choice-chamber used in this experiment prevented any contact being made with potential hosts.
Larval by-products in the form of frass may produce the attractant chemical stimuli, as may the action of bacteria and fungi which attack the medium after the larvae have fed on it. Larval by-products are thought to be the most likely explanation for the results obtained in this study. Stafford, Pitts and Webb (1984) in their study of the host seeking behaviour of Spalangia endius (Walker), a pteromalid parasitoid of the house fly libisca domestica (L.) (Diptera:Muscidae), found a similar ability. Medium containing or having contained house-fly larvae was more attractive to the parasitoids than host-free medium. House-fly pupae
(the host stage attacked by the parasitoid) on their own were not attractive. In this example it would appear that after an initial loca- tion of fly habitats by fermentation volatiles, the fly larvae are located by their larval excretion which in turn elicits the release of searching activity for the pupal hosts. In the present study, infested swedes, as a result of larval attack, decayed considerably faster than non-infested ones, but as the results show, 1%rapae appeared to be able to distinguish the odour of naturally rotting swede from that of one decaying due to larval infestation. Nasonia vitripennis also shows this ability, and will differentiate between liver attacked by host larvae and that decomposing as a result of bacterial action. There is negligible attraction to the latter (Edwards,1954).
Such experimental studies cannot be used to determine the type of
locomotory behaviour elicited by chemical stimuli from treatments such Substrate:
A Moist filter paper
B Washed 3-day old larvae
C Unwashed 3-day old larvae
D 3-day old swede disc
E 3-day old swede disc with larvae
Total time spent on patch
A B CD E
Time spent stationary on patch
A B CD E
Number of stops on patch
A BCD E
Average speed on patch
A BCD E
Figure 2.11 Graphical representation of data given in
Table 2.8. Underlined values do not differ
significantly, p > 0.05. (Difference between
means tested for significance using least
significant difference test.) - 56 - as those already described (Kennedy,1977). In a detailed study of the locomotory response of V.canescens to a contact chemical produced by its host, Waage (1978) found that the parasitoid exhibited a complex orthokinetic response that involved stopping, walking at a reduced rate and probing with the ovipositor. In response to the removal or dis- appearance of the chemical stimulus, the wasp exhibited a klinotactic response which greatly increased the time spent on a patch of contact chemical.
Analysis of the results of Experiment 2 (Table 2.8) allows comparisons to be made of the effect of various substrates on the behaviour of T.rapae. These data are presented graphically in Figure
2.11, pairs of means that do not differ significantly (least significant difference test, p > 0.05) being underlined. The presence of unwashed larvae, or swede (substrates C, D or E) resulted in the parasitoids spending significantly more of their foraging time in the area directly above the substrate than when naked, washed larvae or moist filter paper were presented. Also, in the presence of these three substrates the parasitoid wasps moved at a slower rate than with the remaining two and, as Table 2.9 illustrates, their rate of walking was significantly slower
than when outside the patch area. More time was spent motionless on
these three areas and there was a significant increase in the number
of stops. Although not measured, the intensity of attempts to probe
through the mesh of the arena also appeared to be far higher on these
three substrates. When rate of movement and the number of stops were
considered, no difference was observed between the three substrates.
However, 3 day-old swede infested with host larvae elicited a significant
increase in the time spent on the patch area.
It is obvious that T.rapae was exhibiting a strong orthokinetic
response to some stimuli, the results from this experiment strongly
suggesting that this chemostimulant may have arisen from swede, or Figure 2.12 Diagram of path taken by female Trybliographa
rapae when walking above swede in which cabbage
root fly larvae had been burrowing for 3 days
prior to the experiment. ( • denotes where
wasp paused.) - 58 -
Brassica in general, tissues, particularly when the swede was infested with larvae. Along with V.canescens (discussed earlier in this Chapter) such responses have been noted for numerous other parasitoid species, such as the two ichneumonid species D.putchellus (Noyes,1974) and
Compoletis sonorensis (Cam.) (Wilson, Ridgway and Vinson,1974), the scelionid Triasolcus viktorovi (Kozlov) (Buleza,1973), and the braconid species Aricroplitis croceipes (Cresson) (Lewis and Jones,1971) and
Asobara tabida (Nees.) (Galis and van Alphen,1981).
In addition to this decrease in speed of walking, or actual stopping,
(i.e. an orthokinetic response) many chemicals appear to elicit an
increase in the rate of turning. Waage (1978) investigated whether
this turning in V.canescens was random in orientation (klinokinesis),
or directed (klinotaxis). It was found to be a klinotactic response
tending to turn the wasp back to the patch. The present set of experi-
ments did not involve such detailed observations but, by following the
wasp's path, it was observed that on reaching the edge of the substrate
area the wasp turned, bringing itself back into the area of the chemo-
stimulant (Figure 2.12).
In conclusion, while volatile chemicals emanating from the host
plant may provide the attractant chemical stimuli, it seems likely that
any arrestment response is probably the effect of the combination of
host frass and changes in the host medium as a result of the presence
of the cabbage root fly larvae. Trybliographa rapae exhibited an
orthokinetic response to the presentation of stimulus, this involving
stopping, slowed walking and increased probing, and a klinotactic
response to the disappearance of the stimulus, turning the wasp back
onto the area. -59-
2.6 Aleochara bilineata (Gyn.)
2.6.1 Life history of Aleochara bilineata.
Unusual in being a staphylinid parasitoid, the life history of
Aleochara bilineata (Gyn..) demands further consideration. In his
monograph on the species, Wadsworth (1915) noted that the parasitoid's
eggs are deposited in the soil, in most cases near the roots of
cruciferous plants attacked by larvae of D.radicum. The larvae eclose
in 10 - 12 days and are very active searchers. They are negatively
phototactic, and their natural habitat is below the surface of the
soil at the level where cabbage root fly puparia are found.
To complete their development it is essential that the larvae
enter dipterous puparia. Wishart (1957) has recorded their presence within puparia of D.goratis, D.goritega (Zetter.) and D.platura, as well as D.radicum. Putnam (1959) studied the behaviour of the larvae and found that host finding movements were apparently random in the sense that they were not directed by stimuli from the hosts. This has been supported by work carried out by P.M. Reader (unpublished data).
However, Putnam found that on being presented with equal numbers of
Calliphora spp. (Diptera:Calliphoridae) and D.radicum puparia the larvae could distinguish unsuitable hosts (Calliphora spp.) and, to a large extent, refrain from attacking them.
On finding a potential host the larva proceeds to gnaw a hole in the hardened wall of the puparium. This usually results in a circular hole measuring 0.08 - 0.13 mm in diameter. On entering, the hole is filled up with a white, opaque substance. It is essential that the puparium is sealed to avoid exposure to the air. Otherwise, Nematodes and fungal spores enter, destroying both the host and the parasitoid. - 60 -
After entering, the larva moves very slowly over the pupa and usually confines itself to the anterior, dorsal region of the host. The larvae are thought to make minute punctures in the pupal cuticle with their mandibles and ingest the semi-fluid content.
The first instar larva matures in eight days. The second instar bears little resemblance to the active first instar, being truly para- sitic in appearance. The second instar feeds through a small puncture on the vertex of the head of the pupa, with its body resting on the thorax. This stadium lasts for five days. The third instar feeds very voraciously and is mature within six days. After a quiescent period of
36 hours, moulting occurs, revealing the pupa. The pupal stage is
completed with 14 days and the adult beetle emerges by gnawing an exit
hole in the ventro-cephalic wall of the puparium.
It has been observed that more than one first instar larva may enter
the host puparium. de Wilde (1947b.) reported that as many as five
larvae of A.bilineata may be found within a single puparium. Only one
survives, the others dying soon after entering. The survivor usually
completes its development successfully (Colhoun,1953). It is the first
instar larva that overwinters within the puparium and Colhoun found that
it became active and fed on the host pupa within 24 hours of being
removed from storage at 0°C for three months.
The life history of A.bipustulata (L.) is similar to that of
A.bilineata. Distinguished by two red marks on its elytra, A.bipustulata
is chiefly parasitic on pupae of the bean seed fly maggot, D.platura,
but is also successful on the cabbage root fly (Nair and McEwen,1975).
Observations made at Silwood Park by P.M. Reader (pers.comm.) as part
of a study on the foraging behaviour of, and patterns of parasitism by,
cabbage root fly parasitoids have shown, over a period of four years, - 61 - that A.bilineata is by far the most numerous in overwintering pupal samples. While Wishart (1957) suggested that a relatively hard pupal cuticle deters A.bipustulata from parasitising D.radicum, Finch and
Collier (1984) explained the absence of A.bipustulata from their over- wintering samples at N.V.R.S. by noting that this patitoid occurred earlier in the season than A.bilineata. Both first and second genera- tions of D.radicum were parasitised at Wellesbourne by Aleochara species in 1982, mostly by A.bipustulata. The absence of A.bipustulata from overwintering pupae may be explained by the fact that few second genera- tion pupae have contributed to the overwintering population at
Wellesbourne, Warwick in recent years. They also found, from sequential soil samples collected during the winter, that A.bipustuLata overwinters in the soil as the adult beetle.
2.6.2 Culturing of Aleochara bilineata.
Aleochara bilineata was cultured following B. Bromand (pers.comm.).
Adult staphylinids were placed in plastic sandwich boxes measuring
10 cm x 5.5 cm x 3.5 cm. The floor of the container was covered with a
2 cm layer of sand in which eggs were readily laid. Newly formed cabbage root fly pupae were positioned in the sand and the young staphylinid larvae, on hatching from the eggs, readily found and parasitised the potential hosts. Swede slices and approximately 5 g of minced meat, renewed every two weeks, were also provided. After two weeks the egg-laying adults were removed and placed in another similar container. The parasitised pupae were allowed to develop and staphylinid adults emerged within 4 - 5 weeks. The level of parasitism showed con- siderable variation and B. Bromand (pers.comm.) reports that only about
10 per cent of the maximum number of eggs that can be laid develop into adults. - 62 -
CHAPTER 3
HOST DENSITY AND ITS EFFECT ON LEVELS OF
PARASITISM BY Trybliographa rapae.
This chapter aims to explore the relationship between the number of
cabbage root fly larvae parasitised per female T.rapae and host density;
that is, the functional response. Such a relationship, although simplis-
tic in nature, is of considerable importance, being crucial for the
prediction of the effects of parasitism on population dynamics and the
rate at which these effects take place. The first section introduces the
three major types of functional response and briefly considers the
theoretical background to these models and their implication to host-
parasitoid interactions. The responses of T.rapae to the three potential
host instars and to different host habitats are then explored and an
attempt made to describe them. The next section considers the development
of these functional response models to incorporate two host types, the
resulting model being used to explore any host preference shown by T.rapae.
Finally, the phenomena of superparasitism and multiparasitism are explored.
3.1 Functional Responses.
It was Solomon (1949) who introduced the terms 'functional response'
and 'numerical response' to describe two components of predator-prey
interactions, which can also easily be related to host-parasitoid inter-
actions. He defined the functional response as the relationship between
the number of prey consumed per predator (or host per parasitoid) and the
prey (or host) density. The numerical response describes the relationship
between the numbers of predators (or parasitoids)and prey (host)density.
The relevance of laboratory derived functional responses in nature has been questioned. In a field situation a parasitoid will move between - 63 - areas which contain hosts at different densities. A laboratory experi- ment where a single parasitoid is confined within a small arena, with uniformly sized hosts, appears to be somewhat meaningless under field conditions. Traditionally the parasitoid is allowed to interact with its host for a prescribed period of time. van Lenteren and Bakker (1976,
1978) showed that such an experimental design resulted in a distorted picture of what would probably occur in nature. Parasitoid wasps would not return several times to a site already searched and found unrewording, and a more realistic response might be obtained if the experiment was terminated when the parasitoid first left the host-containing medium.
However, the former method remains the classical means of determining the way in which the predation-rate of predators, herbivores or parasitoids is influenced by prey availability. It provides not only information on the maximum consumption rate of the individual but enables the comparison of efficiencies between species or under different environmental conditions.
Holling (1959a.) recognised three distinct types of functional responses (Figure 3.1): Type 1 where there is a linear increase to a plateau, Type 2 where the response shows a negatively accelerating rise towards an upper plateau and Type 3, a sigmoid response. These three types of functional responses are briefly discussed below (see Hassell
(1978) for full details). The relationship between the density of cabbage root fly larvae and the attack rate of a single T.rapae female is then explored using different host larval instar stages and different Brassica plants.
3.1.1 Type 1 Functional Response.
A response of this kind (Figure 3.1) occurs when the parasitoid attacks hosts in direct proportion to their abundance until limited by their egg supply or some other physiological constraint. It is a Type 1
Type 2
Type 3
b Prey density.
Figure 3.1 The three types of functional response to host
density proposed by Holling (1959a.). Only Type 3
yields density dependent mortality, over the
interval a - b; if the plateau of Type 1 is ignored
the linear relationship describes a i blichasonian' (1933)
parasitoid. - 65 -
response more characteristic of predators which feed continuously until
satiated, at which point feeding stops, giving rise to a plateau. Such
responses are typical of filter feeders and have been shown to describe
the feeding behaviour of Daphnia magna (Straus.) (Crustacea:Diplostraca)
on yeast, Saccharomyces cerevisiae (Meyen ex Hansen) (Fungi:Ascomycotina)
(Rigler,1961).
This assumption of a linear functional response is implicit in both
the Nicholson-Bailey (1935) and Lotka-Volterra (1925 and 1926) models,
with the added assumption that parasitoids do not run out of eggs, or that
predators do not become satiated. If a parasitoid searches for a fixed
number of hosts N over a time period T, the response can be described t' by the equation
Ne /Pt = a' T Nt 3.1
where N /P is the number of encounters with hosts per parasitoid e t and a' is the instantaneous search rate, the proportion of hosts
encountered per parasitoid, per unit time. Assuming T to be equivalent
to the parasitoid's searching lifetime, a'T is identical to the Nicholsonian
(1933) 'area of discovery', a, which may be taken as the proportion of total
hosts encountered by a parasitoid during that time period.
By assuming that the encounters, Ne , are distributed randomly among
the available hosts (Thompson,1924; Nicholson,1933),the number of hosts
attacked, Na , is given by
Na = Nt [1 - exp (- Ne /Nd] • 3.2
By substituting Equation 3.1 this becomes
N = N [1 - exp T P )] . a t t 3.3 - 66 -
3.1.2 Type 2 Functional Response.
The implicit form of functional response in Equation 3.3 assumes a constant searching time. For parasitoids, and most predators, this cannot be so as time is spent on each host (or prey). It therefore follows that as the number of hosts attacked in a fixed time interval increases, the proportion of time available for searching will decrease.
Holling (1959b.) argued that while the time taken subduing and para- sitising each host, the handling time, Th , is constant, at high host densities the sum of these handling times takes up an increasing propor- tion of the parasitoid's time. The actual searching time, Ts , is determined by the number of hosts encountered,
T = T - T N0/P 3.4 s h ( t ).
By substituting Ts for T in Equation 3.1 and rearranging, Rolling's
(1959b.) disc equation is obtained, T a' N t Ne /Pt - 3.5 (1+a' T N ) h t
Type 2 responses differ from the linear form discussed above in that the value for the area of discovery, a, decreases as host density rises. However, the instantaneous rate, a', and T remain constant,
T/T defining the maximum number of hosts that can be parasitised and a' determining how rapidly the curve approaches this upper asymptote.
As with Type 1 responses it is the number of encounters with a constant host density that is being recorded rather than the actual number of hosts parasitised. By the same reasoning as leads to
Equation 3.2, Equation 3.5 leads to Equation 3.6, the Random Parasitoid
Equation (Royama,1971a.; Rogers,1972),
- a' T P, N = N { 1 - exp [ 3.6 a t (1 + a' T N ) h t - 67 - thus expressing the relationship in terms of hosts attacked. It is assumed that a parasitised host will remain exposed to further encounters by the foraging parasitoid and that a re-encounter has the same handling time as the previous one, regardless of whether or not further eggs are laid. On the other hand, prey density does not remain constant during a predator-prey interaction, individual prey items being removed by predation. The equation then becomes
Na N = N 1 - exp [- a' Pt (T-Th ) ]) , 3.7 a t the Random Predator Equation.
Both equations provide good, simple descriptions of the Type 2 functional response when based on random search by parasitoids and predators, and when the parameters describing searching efficiency and handling time are constant.
A survey carried out by Hassell (1978) showed the range of the measured ratio of T /T to be from less than 0.001 to 0.1 for parasitoids and from less than 0.001 to 0.005 for predators. Using this as evidence
Putman and Wratten (1984) have argued that the frequency of Type 2 responses with, very often, good fits between experimental data and model, may arise as a result of satiation rather than limitation by
handling time. Work done by Mills (1982) incorporating the components
of satiation still gives rise to a Type 2 response similar in properties
to the model of Rogers (1972).
Recently, Arditi (1983) has modified the classical 'disc model'
to describe those parasitoids that are able to discriminate between
healthy and parasitised hosts. Previously, equal handling times have
been assumed for both host types. Although often an adequate assumption,
it has been found that handling time is often reduced when superparasitism - 68 - is avoided, for example, the ichneumonid Venturia canescens (Cook,1977) and the pteromalids Nasonia vitripennis (Walker) (Wylie,1965;1970),
Spalangia cameroni (Perk) (Wylie,1972) and MUscidifurax zaraptor
(Kogan and Legner) (Wylie,1971). It its general form, Arditi's model is given by - a' (P T - (T - T) N) t P a N = N { 1 - exp [ a t 11, 3.8 1 + a' T P Nt where T and T H represent the different handling times for healthy and unhealthy hosts respectively. The 'Random Predator Equation' and
'Random Parasitoid Equation' are now special cases when T = 0 and T =
T respectively. The model is therefore seen to unify the treatment of H' predation and parasitism and can also be modified to generate other types of functional responses.
Griffiths and Holling (1969) argued that models based on random parasitoid search were invalid, host populations rarely being distributed randomly. But, as Rogers (1972) pointed out, in their criticism of random parasitoid search models, Griffiths and Rolling failed to realise that the number of attacks carried out during random search and the number of hosts parasitised, while being functions of the host density, are independent of host distribution. In their model, Griffiths and Rolling considered a situation where some hosts were attacked disproportionately more than expected if the parasitoids searched at random. To describe such a pattern of attacks they based their model on the negative binomial distribution. The negative binomial is described by two parameters, the mean and k, an index of aggregation which varies from infinity to zero with increasing aggregation. The number of hosts attacked is given by the equation Ne -k Na = Nt [ 1 - (1 + 17m ) 3.9 and, by substituting Holling's disc equation for Ne/Nt , Yields the functional response equation a' T P -k t N=N [ 1 - (1 + ) I. 3.10 at (1 + a' T )k h Nt - 69 -
3. 1. 3 Type 3 Functional Response.
Holling (1959a.) recorded sigmoid, or Type 3, functional responses
when small mammals were fed on sawfly cocoons. Until relatively recently
it had been assumed that sigmoid functional responses were typical of
vertebrate predation, Type 2 being characteristic of invertebrates.
Both van Lenteren and Bakker (1976) and Hassell, Lawton and Beddington
(1977) have argued that sigmoid responses are also common among arthropod
parasitoids and predators. They attribute their late discovery in host-
parasitoid and predator-prey interactions to experiments usually having
been done in small, simple, laboratory systems. van Lenteren and Bakker
(1976) showed that past experimental design forced the parasitoid to
remain with the hosts in circumstances under which it would normally
emigrate. Thus, the parasitoid was found to search repeatedly substrates
supporting low host densities, increasing the likelihood of finding the
few hosts present. This, along with the observation that even the lowest host densities may have been too high to detect the increasing attack rate of the parasitoid at the lower densities, confounded the interpreta-
tion of a parasitoid's functional response. Thus the sigmoid response
(Type 3) was obscured. Hassell, Lawton and Beddington (1977) attributed the sigmoid response to both parasitoids and predators tending to search more actively with increasing host or prey density. Other experimental evidence for the occurrence of a sigmoid response to prey density in invertebrates comes from the work of van Lenteren and Bakker (1978),
Akre and Johnson (1979), Dransfield (1979), Collins, Ward and Dixon
(1981) and van Alphen and van Harsel (1982).
At least three different phenomena can induce Type 3 responses
(Hasse11,1978; Collins, Ward and Dixon,1981); an increase of a' with
N an increase of T with or a decrease of T with N . Hassell et al. t' Mt h t (1977) described an interaction where only a' varied with prey density,
- 70 -
which they assumed did so in the following manner,
/ (1 + cN ) 3.11 a' = b Nt t
where b are c are constants. The sigmoid analogue of Holling's equation
can now be obtained by substituting Equation 3.11 into Equation 3.5
giving
N b N2 e _ t T 3.12 2 P t l+cN +bT N t h t
To express this in terms of the number of prey attacked Na , rather than
in terms of the number of encounters, Al, certain assumptions are made. e With parasitoids, hosts remain to be subsequently re-encountered,
b T N P t t N = N [ 1 - exp ( )1. 3.13 a t 2 1 + c N + b T AT t h t
For predators that deplete the prey number, when a' depends on the
initial prey density,
b N P TN t t a N = N [ 1 - exp { ( T ) 1 a t 3.14 1 + c N t Pt
but when a' is determined by the number of prey available at any
moment
bP T N N t h a a N = N [ 1 - exp { ( T - 3.15 a t P b N P OY -N ) ) I t t t ta - 71 -
3.1.4 Estimating parameter values.
Estimating the values of the parameters a' and T from the functional h response is important yet fraught with difficulties. Rogers (1972) suggests the use of a linear regression of transformed data to estimate the values of a' and Cock (1977) however believes such a method to T12. be fraught with statistical problems, yielding biased estimates of the parameters. Hassell (1978) suggests the use of a standard non-linear least-squares estimating technique applied directly to untransformed data as a means of estimating the values of these parameters. More recently,
Livdahl and Stiven (1983) have argued that the appropriately transformed disc equation (they suggest the use of the Lineweaver-Burklinearisation) is more amenable to linear regression techniques as it is less likely to violate assumptions than the Random Parasitoid or Predator Equations. A major drawback however, is that the parameters obtained may be less informative in biological terms as an instantaneous equation is used to describe the results of a finite period of exposure for the interaction.
They also comment that the biologically reasonable Random Predator Equa- tion requires the use of non-linear techniques in which statistical comparisons of fitted parameters among predator or prey populations are not easy to perform. However, Williams and Juliano (1985) believe that the use of the method advocated by Livdahl and Stiven produces highly variable and often biased results. They conclude that the best parameter estimates are obtained using the non-linear least-squares method.
This yields unbiased estimates even when the assumption of constant variance is violated.
Recently, Houck and Strauss (1985) have commented that various
researchers have conventionally focused on graphical and mathematical
descriptions of functional responses with little attention being given
to attempting to compare accumulating data sets. One reason for this - 72-
is the lack of standardisation of design and the lack of congruence between design and subsequent data analysis. Using Holling's (1959b.)
generalised model of a functional response they describe an experimental design compatible with the model's assumptions. This includes holding
T constant within trials and across all experimental densities tested; keeping at least either host density (a function of host number) or the
size and shape of the test arena constant so as not to confound the effect of the two; ideally the effective host density should not change
significantly during the trial (of particular relevance to predator-prey
systems); all parasitoids should be consistently exposed to some stan-
dardised set of pre-trial conditions and all individual parasitoids
should be tested only once to avoid secondary experimental conditioning
and to ensure independence of experimental trials.
3.1 . 5 Variation with Experimental design.
As discussed above, Hassell, Lawton and Beddington (1977) suggest
that the prevalence of Type 2 functional responses in experimental data
probably stems from the fact that invertebrate functional responses are
usually obtained from small, simple experimental arenas, using the
preferred hosts. As a result of enclosing the parasitoids within a
relatively small environment the chances that, even at the lowest densities,
hosts will be found and parasitised may become quite considerable. Con-
sequently, the sigmoid section of the curve may be affected giving the
impression of a Type 2 response. Luck, van Lenteren, Kuenek, Twine and
Unruh (1979) found that by modifying Holling's (1959b.) experiment and
prescribing an initial period of search time, during which a host must
be contacted or otherwise the parasitoid emigrates from the search area,
a sigmoid functional response was generated. Such a strategy clearly
minimises the energy spent per offspring in searching microhabitats in
which hosts are scarce or absent. Other workers have shown that by making - 73- changes in experimental design, different results may be obtained both
in the form of the functional response and in the estimated values of
the parameters. Such differences have very different ecological
implications.
Hofsvang and Hagver (1983) explored the functional responses of the parasitoid Ephedrus cerasicola (Stary), an aphidiid parasitoid of
ItIVzus persicae (Homoptera:Aphididae), on a paprika plant over three different time periods. The response after one hour was described by the Random Parasitoid Equation. After six hours, the response was linear, but showed a slight sigmoid trend. High levels of superparasitism were obtained after 24 hours but the curve showed tendencies to exhibit a
Type 2 response. van Lenteren and Bakker (1978) showed that the cynipid
Leptopilina heterotoma (Thompson) (= Pseudeucoila bochei (Weld)) exhibited a Type 2 functional response when confined with its host for one hour but a Type 3 response if the experiment terminated when the parasitoid left the host medium. Collins, Ward and Dixon (1981) made similar observations on the functional response of the aphelinid
Aphelinus thomsoni (Graham) to its host, Drepanosiphum platanoidis
(Schrank.) (Homoptera:Aphididae).
By obtaining functional responses for a range of predator (the damsel fly, Ischnura elegans (van der Linden) (Odonata:Coenagriidae)) and prey ( Daphnia magna (Straus.) (Crustacea:Daphnidae)) sizes,
Thompson (1975) showed that a' tended to decline and Th to increase as prey became larger or predators smaller. Similarly, Fernando and Hassell
(1980), while exploring a variety of responses of the predatory phytoseiid mite, Phytoseiulus persimilis (Athias-Henriot), feeding upon a tetranychid species, Tetranychus urticae (Kock), found that the estimates of attack rate, a', and handling time, Th , also showed some pronounced trends. There was a very clear decrease in Th with smaller prey and larger predators and - 74 - also deutonymph P.persimilis tended to have a higher a' value than protonymphs. Adult females had the lowest attack rates of all.
Physical factors may also affect the estimated parameter values.
Everson (1980), in a study of P.persimilis found that estimates of handling time decreased as environmental temperature rose from 15 to 30°C.
Over the same temperature range the attack rate, a', showed a marked increase. Everson argued that increased temperature resulted in an increased energy demand which was translated behaviourally to hunger.
The speed of a predator increased with hunger, thus reducing handling
time, while the rate of successful prey capture described by the attack
rate increased with energy demand.
Carter, Sutherland and Dixon (1984) concluded that plant structure
was an important factor in determining the quality of a habitat for the
coccinellid Coccinella septempunctata (L.). To determine the effect of
plant structure on the searching efficiency of the coccinellid larvae,
their functional responses on pea and bean plants were compared. It
was found that the attack coefficient, a', was lower on pea than on bean
plants and that this was not due to a difference in the coincidence of
prey distribution and predator searching effort, but to larvae falling
off the smooth leaves of pea plants significantly more frequently than
off bean plants. Similarly, Gardner and Dixon (1985) showed how plant
structure affected the foraging success of Aphidius rhopalosiphi
(Destefani-Perez) (Hymenoptera:Aphidiidae) on wheat. Although
A.rhopaZosiphi can successfully parasitise the four principal aphid
species found on wheat, aphids feeding on the ear were parasitised less
successfully as their position between the grains protected them from
parasitoid attack. - 75 -
3.1.6 Population models and stability.
The majority of models describing the effect of parasitoids on
host population dynamics are elaborations of a basic form,
N AN P ) 3.16 t+1 tt' t
P = c N [ 1 - (W P) ] 3.17 t V
where A is the net rate of increase of the host per generation and c is
the average number of parasitoid progeny produced per host attacked. The
function i(N P ) defines the survival of hosts from parasitism and for t' t the three types of parasitoid functional response curves described above
is given by
Type 1 exp (-12' T Pt ) 3.18
( - a' T Pt ) Type 2 3.19 -x13 (1+a' ) Tet
- b T N P t t ) Type 3 • 3.20 2) exP ( 1+ cNt + b Tet
Past work has tended to suggest that for parasitoids the Type 2
response is the most common. Hassell and May (1973) showed that Type 2 functional responses always contribute to the instability of both host- parasitoid and predator-prey populations. The longer the duration of handling time, Th , in relation to T, the greater the instability, as larger values of Th make the relationship more strongly inversely density dependent.
The upward sweeping part of the curve of a Type 3 functional response (from a to b in Figure 3.1), where increases in host density lead to increases in the level of parasitism on the host population, is - 76 - a density dependent process. Of the three types of functional response it is only such a sigmoid response that is capable of having a potentially stabilising effect on the interaction. Oaten and Murdoch (1975) and
Murdoch (1977) showed, theoretically, that sigmoid responses could indeed be stabilising factors in the differential Lotka-Volterra model.
In this model the most important parameter affecting stability was the amount of time spent in travelling between the patches - 'transit time'.
Hassell and Comins (1978) showed that, on its own, a sigmoid response could not stabilise a difference model of the form given by Equations
3.16 and 3.17. They explained the inability of any form of functional response to stabilise an interaction as being the result of the time- delay (i.e. one generation) between changes in the parasitoid density and the level of host mortality. In the case of most host-parasitoid inter- actions where the parasitoid is specific to, and synchronised with its hosts, the time-delay is of considerable importance. Nunney (1980), however, demonstrated that in a model which included the ability of parasitoids to discriminate between parasitised and unparasitised hosts a sigmoid functional response does have a stabilising effect. Even when the sigmoid functional response cannot stabilise a system by itself, the presence of such a response adds to the likelihood of stability when other density dependent factors operate on the system.
Predators can be classified, according to their diet width, as monophagous (feeding on a single prey type), oligophagous (feeding on a
few prey types) or polyphagous (feeding on many prey types). A mono-
phagous predator is likely to be closely linked to the distribution and abundance of its prey, while a polyphage is unlikely to have its
abundance determined by any individual prey type. For such 'generalist'
predators sigmoid responses may be a powerful stabilising mechanism.
****** - 77 -
The experiments described in the following section set out to explore whether the form of the functional response of T.rapae varies when provided with different host instars of D.radicum and also when the host is presented on three different host plants.
3.2 Experiment to determine the functional response of
Trybliographa rapae in the presence of different host
instars and on different plant substrates.
3.2.1 Materials and Methods.
The Host.
Delia radicum were obtained from laboratory cultures maintained as described in the previous Chapter. All experiments were carried out in a constant environment room (20± 1°C and 70± 5 per cent relative humidity).
First instar larvae were removed from culture 0 - 12 hours after hatching, second instar larvae 5 - 5.5 days after hatching and third instar larvae
14 - 14.5 days after hatching. They were then left on the host plants
(swede discs (35 mm diameter), radishes and Brussels sprouts) for 24 hours before being used in the experiment. Larvae were introduced in densities ranging from 5 to 50 per host plant. Each density was replicated ten times.
The Parasitoid.
Parasitoid females were removed from culture 0 - 12 hours after emerging and placed in small glass tubes with two males, a carbohydrate nutrient source and an excess of D.radicum larvae. Although experience has been shown to be of considerable importance in the foraging efficiency of some parasitoids (for example, Samson-Boshuizen, van Lenteren and
Bakker, 1974), as Table 3.1 illustrates, in the case of T.rapae there was — 78 —
11 a) U • • • a)0 0 •-- 0 ..-1 1.4 +I -H -H a) Ca. 0:1 ON ...— se • • a) r-- 1", Cr) o 0 VI I-1
N V) ON a) • • • 4-1 U •-- w— 0 0 a) -H -H +I • o4 P 11-) -..i. .— a) • • Cu I', r-• c•-n X Lz.1
a) C) ON ON 0 . . n. a) 0 0 0 -.-1 14 -H +I +I a) 04 .— cm X a) LI1 0 ..— i—i
II ce) cf) a) . . %D. c.) .— .— 0 0 a) +I +I +I -,-1 F4 co 0 a) Ca. NO NO •-- 54 41
"cl a) C) -.1 c-n 0 . . -.1. a) 0 0 0 -.-1 14 +I +1 +1 a) 0. .— ce) X . . in. a) .— .— 0 0 Lt-1 H
II ...1- in a) . . -.1. -1-1 c.) 0 0 0 0 a) +t -H +I --I I-. 0• -4- a) . . -4. CI. 0 .— 0 54 Cx1
4.) 0 11 in 0 1.4 P c.) -.4 -.4 al .0 44 Cl) E-4 - 79 -
no significant difference in the number of hosts parasitised by exper-
ienced and inexperienced wasps over a 48 hour period. However, wasps
being standardised were provided with suitable hosts prior to the
experiment, thus eliminating any difficulties that may have occurred
when the wasps encountered their first experimental hosts. The wasps
were used 12 hours later.
The Arenas.
Different arenas were used for the two sets of experiments:
Experiment 3.1
The arenas were plastic butter dishes similar to those used
previously (Figure 3.2a.) with a moistened filter paper on the bottom.
A carbohydrate nutrient source was provided in the form of a ball of
cotton wool soaked in 10 per cent sucrose solution. Larvae were intro-
duced in a swede disc in which they had been burrowing during the
previous 24 hours. A female wasp was placed in each butter dish and
allowed to search for hosts over a 48 hour period.
Experiment 3.2
Soil was sieved (4 mesh/cm) into plastic plant pots (10 cm diameter).
The soil was dampened and each plant placed centrally in individual pots.
Radishes (cv. Cherry Belle (Clause)), six weeks after sowing (root dia- meter, approximately 2 cm) were planted leaving about one third of the swollen root exposed. Brussels sprouts plants (cv. Winter Harvest) of a similar age were positioned so that the soil covered all their roots.
Swede discs were placed in a central position on the soil surface.
Having been left for 24 hours after potting, second instar D.radicum were transferred from culture onto the soil around the plant base. Any dead larvae found on the soil surface after a further 24 hours were a.
swede disc cotton wool on moist soaked in filter paper sucrose 177777A 0 solution
b.
transparent gauze covered perspex top i hole
experimental plant
plastic flower pot
Figure 3.2 Arenas used to obtain functional responses of
Trybliographa rapae on (a.) different larval
instars of Delia radicum (Expt. 3.1) and (b.)
various plant substrates (Expt. 3.2). -81 -
replaced. The pot was then covered with a transparent perspex top with
gauze covered holes for ventilation (Figure 3.2b.). A single standard-
ised female T.rapae was introduced into the experimental arena and left
for 72 hours to interact with the host population. Again, a ball of
cotton wool soaked in sucrose solution was provided as a nutrient source.
Recording of Results.
At the end of each experiment the wasps were removed, the larvae dissected and the presence of parasitoid eggs recorded. As mentioned in
the previous Chapter, to make dissection easier the larvae were left for
24 hours to allow the eggs to become opaque.
3. 2. 2 Results.
The results are displayed graphicallly in Figures 3.3 and 3.4 in terms of the number of hosts parasitised, N plotted against the number a of hosts available, Nt . The model description of these data, however, was not straight-forward. Using a non-linear least-squares computer programme that minimises the sum of squared differences between the observed and predicted results, it was found that a Type 3 response, as modelled by Hassell, Lawton and Beddington (1977), provided the best description of the data. However, except for the results obtained from
the Brussels sprouts experiment, the values for parameter c were found to be negative (Table 3.2).
Searching efficiency, a', in the model is given by Equation 3.11, and by changing the value of c the searching efficiency varies depending
on the host density. If c = 0 searching efficiency is directly propor-
tional to the number of hosts available, the rate at which searching
efficiency increases being given by the parameter b. When c is positive
the attack rate increases with host density towards an upper plateau, Figure 3.3 Functional responses of Trybliographa rapae to
(a.) first, (b.) second and (c.) third larval instars
of Delia radicum. Curves are best fits of the special
case of the Hassell, Lawton and Beddington (1977) model
described in the text, fitted using a non-linear least-
squares computer programme that minimises the sum of
squared differences between observed and predicted
results. a. 12- • • 92 • • • • 92 9- • • • 6 2 •2 •3 92 .3 2 63 *2 •5 • 3 6- • • 2 • 6 92 • 3- • 4•5 413 63 •4 0 10 20 30 40 50
12- • • • .2 • 92 3 9- • • , 2 • 2 e2 • • 2 • • 3 65 92 6- 5 • .2 •3 • 62 •4 •2 •2 3- /•5 .5 / 94 0 • 10 20 30 40 50
12 -
9-
6- • • • 92 S5 • 2 94 3- 63 • 5 .3 • 9300014 e3 4 • .I. • ...... 6.1...... 5. 92 93 2 * • 64 2 0 ( 6 ...—.. 6• ...... 6 0 10 20 30 40 50 Host density.
- 85 -
a. 12 • • 9- 93 • • • .3 3 63 63 • 3 .3 6 63 ,....3 •2 • .2 •2°..- •3 • •
3 - • •7 •2 •2
0 /6-ei 10 210 30 40 50
b. 12-' • 2 13 9 Cu 0 9 - ..... •2 cs3 .4 e4 0 Cu - .4...... /.....2 • • CO a 6- • _....4 CA 62 U o 0/.4 = 3- • •2 15 e2/85 • ... .5 .3 2 .3 E3 0 1 1 I I 1 Z 0 10 20 30 40 50
C. 12- • .2 •2 • • 9- • 93 •3 • • .3 •4 •3 • •3"*...... 03 • • ../.... 6- • e2 .4 • .2/104 •2 e 4 •2 3- •2/.2 63 • /3
0 62 1 10 20 301 410 50
NI-Iost density. - 86 -
In star Parameter values S.S.R.
First 0.02 ± 0.01 -0.08 t 0.01 0.19 ± 0.05 192.82
Second 0.04 ± 0.03 -0.07 ± 0.03 0.14 ± 0.04 149.64
Third 0.01 ± 0.01 -0.05 ± 0.05 0.39 ± 0.27 70.85
Parameter values Substrate S.S.R. T h
Swede disc 0.01 ± 0.005 -0.06 ± 0.01 0.17 ± 0.04 71.77
Brussels sprout 0.11 ± 0.11 0.02 ± 0.14 0.09 ± 0.02 96.30
Radish 0.02 ± 0.01 -0.06 ± 0.02 0.15 ± 0.04 91.36
Table 3.2 Parameter estimates ( ± 95 per cent confidence intervals)
of the functional responses of Trybliographa rapae to
Delia radicum using Hassell, Lawton and Beddington's (1977)
Type 3 model. The sums of squared residuals (S.S.R.) are
also given. C = -0.01 200-,
180-
160-
140-
120- a' 100- C =0.0
80-
60 -
40- C = 0.01 20 -
20 40 60 80 100 120 140 160 180 200
Host density, Nt.
Figure 3.5 Simulated relationships between the search rate,
a', and host density, N t , obtained using Equation
3.11. In all cases b = + 0.5. - 88 - while if c is negative searching efficiency increases at an accelerating rate as shown in Figure 3.5. This last function has no biological interpretation and therefore suggests that the model used was not suitable for these data and should be modified.
If it is assumed that searching efficiency increases linearly with available host density as a result of increased olfactory stimulus from areas containing high host numbers, the model described above may be modified to incorporate this assumption by making c equal to 0.
Searching efficiency, a', is now given by
a' = bN 3.21 t and Equation 3.12 becomes 2 T Ne b N t 3.22 2 • Pt 1 + b ThNt
This special case of the Hassell et al. (1977) model for describing a
Type 3 functional response, where the increase in searching efficiency is directly proportional to the host density, provided a good description of the experimental data (Figures 3.3 and 3.4). In plots of the residuals agains the independent variable, N t , no clear trend was observed, implying that the fit of the data to the model was a satisfactory one (Draper and
Smith, 1966). The parameter values are given in Table 3.3.
3.2.3 Discussion.
In the described laboratory system it was the Type 3, sigmoid functional response that provided the best description of the data.
This lends support to the belief that such responses should not be considered as being atypical of invertebrate predators and parasitoids.
Functional responses of this kind have been shown to exist for Trioxys indicus (Subba Rao and Sharma) (Hymenoptera:Aphidiidae) on Aphis craccivora (Koch) (Hemiptera:Aphididae) (Pandey, Singh, Kumar, Tripathi Parameter values Instar S.S.R. T h
First 0.09 ± 0.05 0.10 ± 0.01 242.25
Second 0.12 ± 0.06 0.11 ± 0.01 160.04
Third 0.01 ± 0.01 0.26 ± 0.05 71.81
Parameter values Substrate S.S.R. T h
Swede disc 0.05 ± 0.01 0.09 ± 0.01 96.12
Brussels sprout 0.09 ± 0.03 0.10 ± 0.01 96.54
Radish 0.06 ± 0.02 0.11 ± 0.01 99.62
Table 3.3 Parameter estimates ( ± 95 per cent confidence intervals)
of the functional responses of Trybliographa rapae to
Delia radicum using a special case of the Hassell, Lawton
and Beddington (1977) model of a Type 3 response (see text
for details). The sums of squared residuals (S.S.R.) are
also given. - 90 - and Sinha, 1982), Venturia canescens on the almond (flour) moth, Ephestia
(Cadra) cautella (Walker) (Lepidoptera:Pyralidae) (Takahashi, 1968) and
Pseudogonatopus flaviftmur (Esaki and Hash) (Hymenoptera:Dryinidae) on the brown planthopper, Nilaparvata lugens (Stal.) (Homoptera:Dalphacidae)
(Chua, Dyck and Pena,1984), as well as those mentioned earlier. If para- sitoids are able to evolve searching strategies that enable them to sample a habitat unit so that minimal time and energy is spent searching those units with little or no hosts, then sigmoid functional responses clearly confer a certain degree of survival advantage on the parasitoids as searching costs are reduced when the number of hosts is small.
The estimates of the attack rate parameter and the handling time,
in Table 3.3 show certain trends. In the first experimental series Th' the time spent to 'handle' the first instar was the shortest, 4.79 hours.
Although actual handling time could not be determined accurately by observation, the calculated value was thought to be considerably higher than the actual time spent parasitising a host. This was a result of no consideration being given to the periods of non-searching activity.
Wishart and Monteith (1954) and L.Vet (pers.comm.) report that, in the case of T.rapae, location of the host larva may require considerable time, but that the act of oviposition does not occupy more than one minute. The time required to 'handle' the third instar was at least double that of the two other host instars. This may be explained by either the increased thickness of the larval skin of the third instar, making it difficult for the parasitoids to insert their ovipositors, or possibly the physiological unsuitability of the third instar for para- sitoid development. Although James (1928) and Moltschanova (1930) reported that only first and second instar cabbage root fly larvae are attacked by T.rapae , the present results indicate that third instar larvae are also parasitised. However, more young larvae are likely to be attacked than older ones as they are more readily accessible. The -91 -
slight difference in the attack rate parameter, b, between first and
second instar may have been the consequence of the older larvae, still
equally acceptable to the parasitoid, being easier to locate and attack
because of their larger size.
One disadvantage of estimating the parameter values, b and Tie
from the functional response model is that they only have any real
meaning in comparisons between identical conditions. Substrate, type of
arena, temperature, humidity, lighting and duration of experiment may
affect the parasitoid's activity patterns and thus influence attack rate
and handling times. This difference is very apparent if the results
obtained for second instar larvae in a swede disc in the two experiments
are compared. Both parameter values were smaller in the second series
of experiments, most notably the value of b. This was probably the
result of the larger arena used and the longer experimental period over
which the interaction occurred.
In Experiment 3.2 there was no apparent difference between the handling times for the various plants. However, the attack rate was lower on both swede disc and radish than on Brussels sprouts plants
(Table 3.3). In the latter, the larvae were to be found within a narrow toot and stem whereas in the swede and radish the larvae were able to burrow to some considerable depth into the plant tissue, thus possibly reducing the rate at which parasitoids encountered potential hosts.
As mentioned above, sigmoid responses can contribute to the stability of a host-parasitoid equilibrium, being density dependent up to some thres- hold host density. Although such functional responses may contribute to some degree in the stabilisation of host-parasitoid interactions in the field, as a result of the time-delayed, one-generation feedback between changes in parasitoid density and in the level of host parasitism, their effect is probably not considerable. - 92 -
3.3 Inter-Age-Class Preference.
3.3.1 Detecting Preference.
When a parasitoid, or a predator, is exposed to two or more host,
or prey, types preference for a particular type and the ability to
switch from one host to another are important aspects of the searching
behaviour. Under natural conditions a host-parasitoid system will be
characterised by each parasitoid individual being faced with a range
of host developmental stages. Using a range of functional responses
will not describe the interaction sufficiently since, as Hassell, Lawton
and Beddington (1976) comment, the ratio of these attacks may or may not
be the same as that predicted from a knowledge of separate functional
responses. There may also be some 'switching' from one host category
to another as the relative abundance of each type changes (Murdoch,1969;
1973; Lawton, Beddington and Bonser,1974; Akre and Johnson,1979).
The searching preference of Anisopteromalus calandrae (Howard)
(Hymenoptera:Pteromalidae) for different stages of its host,
Cal losobruchus maculatus (F.) (Coleoptera:Bruchidae), was explored by
Heong (1981). In preference experiments where two stages of the host were presented to the female parasitoid, Heong showed that a definite preference was exhibited for the fourth instar, followed by the pupa and third instar respectively. Cheng (1985) has shown that the braconid
Diaeretiella rapae (Curtis) exhibits a marked preference for fourth instar and adult Brevicoryne brassicae (L.) (Hemiptera:Aphidoidea) when presented with a population of both old and young instars. Gardner and
Dixon (1985) showed that Aphidius rhopalosiphi exhibited no preference for either Ilkutapolophium dirhodum (Walker) or Sitobium avenae (Fabricius)
(Hemiptera:Aphididae). Interestingly, as the handling time for the latter was significantly longer fewer S.avenae were parasitised even when abundant. - 93 -
In simple terms, preference for a particular host type may be considered to be a disproportionate level of attack on that host when compared to the proportion available in the environment. Hassell (1978) regards such preference to be the result of some combination of differences in searching efficiencies, differences in the time spent in the different habitats or other changes in the foraging parasitoid's behaviour when faced with two, or more, host types.
Cock (1978) proposes the following set of observations for detecting preference:
(1.) Functional response experiments are carried out with each host
separately and the parameter values estimated from the appropriate
functional response equation.
(2.) Any preference resulting from differences in the functional response
parameters can be conveniently displayed in terms of Nail Na2
plotted against Nti / Nt2 or, alternatively, as the proportion of
one of the species or type in the total diet against the proportion
available (e.g. N 1 / (N 1 aagainst N ti/(Nti (The sub- /(Na Na2 Nt2)). scripts 1 and 2 distinguish the terms for the two host types).
Such innate preference will then be detected as a deviation from
a slope of unity passing through the origin.
(3.) Further experiments can then be carried out in which various ratios
of the two host types are presented together.
Cock (1977) reviews a variety of indices of preference that have
been amassed in the literature. Murdoch (1969,1973), for example,
suggested using an appropriate predator model to predict the extent of
preference in the face of two prey types presented together. - 94 -
Using a modified disc equation the number of each prey type eaten is predicted by
a ' T N 1 t1 N - 3.23 al 1a ' T N a ' T N + 1 hl tl + 2 h2 t2 and a' T N 2 t2 3.24 N - a2 1 + a N + a T N 2 Th2 t2 1 hl tl
The ratio of the two prey eaten is therefore given by,
N a 'N al _ 1 ti 3.25 N a N a2 2 t2 a I /a/ I being a measure of preference that is analogous to the index 1 2 proposed by many other workers (c.f. c in Murdoch,1969).
To include the effect of the exploitation of prey during the interval T, Lawton, Beddington and Bonser (1974) and Cock (1977) made use of the Random Predator Equation of Rogers (1972) to predict the number of prey eaten,
3.26 Nai = Nt/ E 1- exP (-a' / (T ThlNal Th2Na2 ))
N = N [ 1 - eXp (-a'2 (T - T N - T N ))] • 3.27 a2 t2 h2 a2 hl al
The ratio of the prey types eaten thus becomes
N N [1 - exp (-02'1 Ts)] al tl 3.28 N N [1 - exp (-nor' T ] a2 t2 2s where T = (T - N - T N ). This model can be used to describe s hl tl h2 t2 preference experiments where exploitation occurs, the preference index being a variable dependent on the time spent searching, T , which in s turn depends on the number of both prey types eaten. - 95 -
Using a similar procedure but basing it on the Random Parasitoid
Equation (Equation 3.6), comparable equations can be derived for a
parasitoid exhibiting the 'special' case of Type 3 functional response
described previously. The preference index then becomes
N N (1 - exp (- b N T )) al t1 1 t1 3 - 3.29 A N (1 - exp (- b N T )) a2 t2 2 t2 s
2 where T = T/ ( 1 + b i Nti Thi + b 2Nt :T722 ), Na l and Na2 being the number s of host types 1 and 2 parasitised respectively. (See Appendix 3 for
derivation of these equations).
Using this model, predicted and observed results can then be compared.
Ideally the procedure should be repeated for a range of total host densi-
ties that encompass those used in the functional response experiments.
Any difference between the predicted preference from the difference in
functional response parameters and the observed preference will then be
due either to an active rejection of one of the hosts or to some change
in parameter values as a result of the parasitoid experiencing the two
host types together.
3.3. 2 Experiment to determine the searching preference of
Trybliographa rapae for different developmental stages
of its host, Delia radicum.
Method.
The experiments were based on the functional response observations made during Experiment 3.1. Over the 48 hour period, the single,
standardised parasitoid searched for a mixture of two host stages
introduced in different ratios, 4:1,3:2,2:3 and 1:4, always to make a total of 25 hosts in each treatment. The host combinations used were
first versus second instar, first versus third instar and second versus - 96 - third instar. As mentioned earlier in the Chapter, there was no significant difference between the number of larvae parasitised by experienced and inexperienced wasps. To avoid the added problem of conditioning of the parasitoid while gaining experience, wasps were not allowed to encounter any potential hosts prior to the experiment.
Results.
As described by Cock (1978), any preference resulting from differences in the functional responses to the different host types can be displayed in terms of Nal /Na2 plotted against Nti /Nt2 . Preference
can then be detected as a deviation from a slope of unity passing through
the origin. These results are presented in Figure 3.6 and the statistical
analysis, that of testing the slope of the regression line passing through
the origin for any deviation from unity using the normal t-test, are given
in Table 3.4. A plot of the proportions, AN + N ) against 1 al a1 a2 could also have been used but, as Heong (1981) states, Nt1 /(Nt1 Nt2)' the normal t-test is not appropriate as the data are confined at the 0
and 1.0 points and residual analysis may be more suitable in this case.
No significant preference (Table 3.4) was shown for either first or
second instars when presented together, both being parasitised in propor-
tions directly dictated by their ratio in the initial host population.
When either first or second instars were presented with the third instar
there was an active selection of the younger developmental stage. Such
a marked preference may arise from the difference between the functional
responses defined earlier for each instar. By substituting the values
estimated for parameters T and b previously into the appropriate equa-
tions (see Appendix 3), the predicted preference on the basis of such a
difference may be obtained. Any deviation from this model indicates
changes which have occurred in the parasitoid's handling time and/or
searching rate as a result of it encountering two host types together. Figure 3.6 Parasitism of Delia radicum by Yrybliographa rapae when
two hosts were presented:
a.) First instar (V1 ) and second instar (N2),
b.) Second instar (N1 ) and third instar (N2),
c.) First instar (N1 ) and third instar (N2).
N and N are the respective numbers of hosts attacked. al a2 The solid line gives the best linear fit for the data
collected, the broken line is the no preference line. a. 10- y = 1.03x
8-
N ai 6- Na2 4- • .2
I 111 2- • e 1,3 2 2...... 23,-- E o--cf 1 I 1 I .1 O 1 2 3 4
b. 10- y = 1.99x • •
C. 10- y = 2.17x • • 8- .3 S • .3 92 63 • Nai 6- • • Na2 4- • • • • :3 • 2- • • 9 2 •.2.. Cs' 0 t o 1 Host 1 Host 2 t d. f. P
1st instar 2nd instar 0.32 38 >0.1
2nd instar 3rd instar 3.85 38 <0.002
1st instar 3rd instar 4.19 38 <0.001
Table 3.4 Analysis of the slope passing through the origin of
Nal /Na2 plotted against Ntl /Nt2' Figure 3.7 Preference in parasitism when two hosts are presented
together. The solid line is the predicted preference
on the basis of the individual functional response,
the broken line is the no preference line.
a.) First instar (N1 ) and second instar (N2).
b.) Second instar (N1 ) and third instar (N2).
c.) First instar (N1 ) and third instar (N2). 1•0 - . 2 _I 0 .8 - :-2 3 :-2 • I/ . d' * 0-6 - • 4-3
0 -4 - /
III' 0 -2 - ol • / • 2.- e_.4 / / 0 -0 0-0 0-2 0.4 0.6 0-8 1.0
TO
Z
0 -6- -0 C 04 - i- C • / 0 / 0 .2 -I f. 0 0. 0 0•0 1 I I a: 0-0 0.2 0-4 0.6 0-8 1-0
1-0 .n•••""...".'.."/77. 0-8 • • / • • / • •2-3 • , / • 2 ./ 0-6 • / / / • • / C . e 0.4 .
0.2
0-0 0-0 0-2 0-4 0-6 0-8 1-0
Nti Proportion N 1 available, .
N ti+ Nt2 - 102-
Using the model described above the predicted proportions, based on the two individual functional responses, were calculated. The observed results are given in Figure 3.7 where (Nor or + N )) has been plotted 1 /(N 1 a2 against Y + N )). In all three cases the model did not provide ( titl t2 2 a good description of the data, yielding values of x that were signifi- cantly higher than those at the 5 per cent probability level (36 d.f.).
There was no significant deviation from the no preference line when first and second instars were presented together (t = 0.111; p > 0.1,
38 d.f.) but, again, when either of the younger instars were presented in a population with third instars there was an obvious selection for the preferred younger stages.
Discussion.
From this analysis it is apparent that, although the parasitoid was able to attack all three instar stages of D.radicum, there was a marked preference for either first or second instar if presented with third instar larvae. No preference was shown between first and second instar larvae.
This preference for the younger larvae may be explained, as mentioned previously, by the increased thickness of the larval skin of the third
instar. This made it difficult for the parasitoids to insert their ovipositors.
Preference may be the result of a combination of innate and
behavioural preference (Cock,1977). The former is the result of the
differences between the functional responses when each instar population
is presented on its own. The latter is due to the active rejection of
one of the host types, or changes in the search parameters as a result of
the parasitoid experiencing the two host types together.
It is interesting to note the form of the predicted curve in
Figure 3.7a. This suggests that, as a result of lack of any preference - 103 - between first and second instars, the parasitoids should have concen- trated more on attacking the more numerous host species. This is the classical 'switching' response (Elton,1927;Murdoch,1969) which occurs when the host (or prey) which is relatively most abundant is attacked supraproportionally, the parasitoid switching from preferring one host stage to preferring the other. Cornell and Pimentel (1978) mention that apart from some suggestive evidence (e.g. Tinbergen,1960;Clarke,1968;
Gibb,1962) an unequivocal case of switching has not been observed under natural conditions. The stabilising characteristics of such a mechanism are therefore largely unknown. Begon and Mortimer (1981) have commented that the actual importance of the density dependent, and hence stabilising, part of the curve is very much dependent on the concavity of the curve in this region and also on the relevance of the host density in the upward sweeping region to a particular field, or laboratory, situation. Cornell
(1976) considers switching to be adaptive to the predator (or parasitoid) regardless of whether prey (or host) populations are stabilised.
Although predicted, such a switching response did not occur when first and second instar larvae were presented together (Figure 3.p.
The proportion of each host population attacked was found to be directly related to its relative abundance in the environment. When second instar larvae were presented to T.rapae in two different host plants (swede and radish), a clear switching response was observed (S.Citrone, unpublished data). Interestingly, the point of switching in this case occurred when the hosts were present in equal numbers in both plants. This suggests that, in reality, little preference existed for either host 'type', the parasitoid sampling the environment to allow detection of which host was more readily available.
Significant deviation from the predicted results indicated that the searching behaviour of the parasitoid was probably different when exposed to an environment with two host types. This was probably due to either - 104-
active rejection of one of the host types or changes in the search
parameters' values as a result of the parasitoid experiencing the two
host types together. Lawton, Beddington and Bonser (1974) have proposed
a method to estimate the search parameters in the multiple host situation.
As well as violating the assumptions of regression analysis, this method
also results in two estimates of the T value and, as Heong (1981) points
out, it is uncertain which is correct.
3.4 Superparasitism.
During the course of these series of experiments it was very notice-
able, during dissection, that only few of the cabbage root fly larvae
contained more than one egg. In fact, of the 13200 larvae dissected only
24 (approx. 0.8 per cent of those parasitised) had more than one egg
inside them. Of these, only 5 had more than two eggs. Being a solitary
wasp, only one T.rapae offspring emerges from each host pupa. It is
therefore adaptive for ovipositing females to discriminate between healthy
and parasitised hosts in such a way that no more than one egg is laid in a
single host larva. Such behaviour reduces egg wastage and is of a selec-
tive advantage.
Rogers (1972) found that V.canescens parasitising Ephestia cautella larvae could detect the presence of a parasitoid egg, and hence avoid superparasitism, within 5 minutes of that egg being laid in a healthy host.
The percentage avoidance increased rapidly over the following minutes, reaching a level of 70 per cent after only 30 minutes of egg development.
Rogers was unable to conclude what V.canescens detects when it stabs a parasitised host, but commented on the existence of many sensillae at the tip of the ovipositor which may detect, chemically, the presence of an egg. van Lenteren (1976) found that for the solitary endoparasitoid
Leptopilina heterotoma, ovipositing in larvae of a Drosophila species, - 105-
the wasp was not only able to discriminate between parasitised and
unparasitised hosts but also between hosts with different numbers of
parasitoid eggs. Superparasitism appeared to be avoided maximally
some 70 seconds after the first oviposition. In this case, the host
was marked during or after the actual egg deposition, probably by
substances from the wasp's abdomen. Eijsackers and Bakker (1971) found
that in cases of superparasitism, supernumerary larvae of L.heterotoma
were sometimes eliminated by direct physical attack. Fisher (1961)
also reported that such attacks occur in V.eanescens, the older larva
always being successful. Finally, van Alphen and Nell (1982) found
that Asobara tabida (Nees) (Braconidae:Alysiinae), another larval para-
sitoid of Drosophilidae, was also able to distinguish unparasitised hosts
from those previously parasitised by themselves or by conspecifics, but,
in contrast to L.heterotoma, could not discriminate between hosts with
different numbers of eggs.
van Lenteren (1976) has suggested a number of possible causes of
superparasitism:
(1.) A female lays more than one egg per oviposition
(2.) A female does not recognise hosts parasitised by other females
(3.) A female lays a second egg within the period needed for building
up a factor that causes avoidance of superparasitism
(4.) Two or more females lay eggs simultaneously in one host
(5.) A female's tendency to oviposit increases when she encounters
only parasitised hosts for a long period, and she will then lay
eggs in these hosts and, finally,
(6.) A female has not yet learnt to discriminate. van Lenteren (1976,1981) suggests that the first four causes seldom play a role in superparasitism and cites numerous examples to support his case. - 106-
Unfortunately, an exhaustive study of superparasitism in T..rapae
could not be made because of the difficulty in actually observing the
wasp parasitising a burrowing host. The following experiment investigates,
in a very simple manner, the level of superparasitism that arises from a
single female T.rapae and also from conspecifics.
Materials and Methods.
A standardised female wasp was allowed to forage and oviposit in
suitable hosts in a butter dish for 24 hours. The hosts, 30 second
instar larvae, were presented in a swede disc. At the end of this
period the wasp was removed. After a fixed period of time ranging from
24 hours after the start of the first encounter period (i.e. immediately
after the end of the first experimental period) to 120 hours later, the
wasps were allowed to search for a further 24 hours. Initially, 40
replicates were set up and each female left for 24 hours before being
removed from the butter dishes. For the second interaction, 20 of these
females were returned to their original dishes (Treatment A.), while
the other 20 were placed in dishes in which they had not previously
foraged (Treatment B.). Wasp and butter dish were allocated using a
random number table. Thus, the result of the presence of the same
individual female parasitoid and a conspecific on levels of super-
parasitism could be explored. At the end of the experiment the larvae
were dissected and the number of parasitoid eggs recorded.
The origin of each egg, as has been previously mentioned, could not
be determined. To serve as a control, 20 standardised female wasps were
allowed to forage for potential hosts for 24 hours. After this period,
the larvae were dissected and of the 66 larvae parasitised only one was superparasitised, containing two eggs. The mean number of larvae para- sitised per relicate was 3.3 ± 0.57 (mean ± 95 per cent confidence intervals). - 107 -
In -7 cg 0 0 ta 0 0 0 0 0 > . . . . 0 00 u sioj +1 +1 +1 -14 44 0 '.....Co 0 1/40 .-- 0 0 0 Do 0 0 0 0 0. 00 . . In cl) C 0 C.) --1 C.1 ON 0 %.0 ..1- -..1• ..1• ...1- Ln .-- .-- n-• .- .-
'CI W CD 4-1 -0 • r4 0.4 CO 14 CO al 1.1 144 cd ..- t..4 o o ii-4 a. CO o 0 0 0 0 .,4 . . . . •t ci) CD > — I-4 0 CO CO co > g '-I +1 +1 +1 +1 +1 P 1.1 to----, O CO 4- CO ,-. -. o o O ,-4 ba O o o o o 4 14-1 CD 60 a.) - - - - ,- .--.. 0 E in co 0 $4 IA • W .40 en en -.I -.../• 0 .0 ts -.I• ...1- lf) in V) V g 0 /41 s.... .-1 Ctl Co 4-1 n1' 0 4..1 1:1 O 0 CO 4 4.1 .--.. .- co 0 • r.1 0 It:3
U V O) ,-1 .13 -la 4-1 1 1.: '4. In. . /:n14 ILI 14 o o o o o U U * 01= w +1 +1 +1 +I +I 4) CO Q. C-1. C13 CO ..- in 11) > W ". 0. cs3. 4-1 I... S. 0 Cu 0 r•-• 1-.. r•-• r•-• r•-• I L. C.) 41 W 1..W0...... /
a) ...• .0 ,-i CA E -51 CO . . -.1. cl). '.° 3 in Ei 0 0 0 0 0 z F; a) 44 -II 41 41 +I -H (7) to a) r•-• r-- '- E ce cl . . . Cu CO r•- es. N. N. 0. VI
4.• I.. U) WI- 4.' .- .4' Co c•I %.0 0 Cu eV -.I- N. cn eV in 0 1.1.3 L• 4-, W 3 1„. -la 0 ea C - 108-
3. 4.2 Results.
As Table 3.5 illustrates, the number of larvae parasitised per replicate did not differ between the two treatments. However, when the average number of eggs per larva was considered, for those periods commencing only 24 and 48 hours after the initial encounter, significantly higher numbers of eggs were found per larva in those attacked by con- specific females. After this initial period there was no subsequent difference between the two treatments.
3. 4.3 Discussion.
Within the confines of the described experimental system there appeared to be some suggestion that, in the case of T.rapae, conspecific females did not show as strong a discriminatory behaviour against hosts parasitised by other females as when encountering a host previously parasitised by themselves. This certainly seemed to be true for the first 48 hours. Subsequent to this initial period discrimination appeared to be equal for hosts parasitised by themselves or by conspecifics.
There are numerous studies which report on the inability of para- sitoids to differentiate between hosts parasitised by themselves and by others of the same species (e.g. Fisher,1971;Rabb and Bradley,1970;
King and Rafai,1970;van Alphen and Ne11,1982). Studies showing the reverse, that parasitoid females tend to avoid superparasitism when their own eggs are already present are rare. Hubbard, Harris and Gow
(unpublished manuscript) showed that V.canescens females were more effi- cient at detecting their own eggs within hosts, and avoiding subsequent superparasitism, than they were at detecting and avoiding eggs of other females. In fact, they found that 'mothers' were about 30 per cent more efficient than 'non-mothers' in detecting prior parasitism and avoiding superparasitism. Legaspi (1984) reported some indications that - 109-
Diadegma fenestralis (Holmgren.) (Hymenoptera:Ichneumonidae) females did not recognise hosts, Plutella sylostella (L.) (Lepidoptera:
Yponomeutidae) larvae, parasitised by conspecific females. Venkatraman
(1964) however claimed that this species did not show any tendencies to avoid superparasitism under any conditions.
When a female belonging to a solitary parasitoid species lays an egg in a previously parasitised host, one egg is always wasted. If an egg is laid in a host previously parasitised by a conspecific, there is a possibility that the offspring from the second egg may survive, usurping the initial egg. Meyer-Gressman (1967) and Eijsackers and Bakker (1971) observed that in L.heterotoma, another cynipid, direct physical attack among supernumerary larvae was an effective anti-superparasitism mechanism. Larvae hatching within a reasonable short time of one another may have a more or less equal chance of survival. Laying a second egg which will hatch considerably later that the first places the supernumerary larva in a less promising position. Ovipositing females may also be able to recognise their own eggs and larvae within hosts sooner than eggs laid by other females. The differences during the initial 48-hour period may be the time required for the factor which causes general avoidance of superparasitism to build up.
3.5 Multiparasitism.
In addition to superparasitism, the population dynamics of T.rapae may also be affected by multiparasitism of a single host by various parasitoid species. AZeochara bilineata and A.bipustulata are the only parasitoids abundant enough to compete with the cynipid (Wishart and
Monteith,1954) and this short section considers the result of parasitism of the same host by A.bilineata and T.rapae. The attack by T.rapae occurs well in advance of that by the beetles. However, both species of
Aleochara feed externally on the pupa and their attack may occur before - 110 - the T.rapae larva leaves the host and assumes an external feeding position.
Wishart and Monteith (1954) state that where a larva of Aleochara spp. has become established in a puparium before the T.rapae larva is in its external position, it feeds on, and eventually kills both the host and the cynipid larva. They found that in all observed cases of multi- parasitism it was the larva of Aleochara spp. that survived.
3. 5.1 Materials and Methods.
To explore the consequences of multiparasitism, A.bilineata larvae were presented with various combinations of unparasitised and parasitised
(by T.rapae) cabbage root fly pupae. The experimental staphylinid larvae were between 1 - 3 days old, work by P.M. Reader (pers.comm.) having shown this to be the optimal age for maximum parasitism. Delia radicum pupae were placed, approximately 1 cm deep, in damp sand in a plastic butter dish (see Chapter 2 for description). The first instar larvae were added and left for 96 hours. This allowed sufficient time for the larvae to locate and parasitise the hosts. The pupae were then examined using a binocular microscope and attacked and parasitised pupae identified and separated. These were then placed in damp sand in glass tubes (5 cm x
2 cm) to complete development. The emerging insects were noted. All observations were carried out at constant environmental conditions of
20 ± 1°C and 70 ± 5 per cent relative humidity.
3. 5. 2 Results and Discussion.
In the initial series of experiments parasitised pupae were used in which T.rapae had assumed its ectoparasitic stage within the host puparium.
This occurs some 4 - 5 days after the host pupates and the parasitoids are recognisable through the puparium. There was a significant difference in
the number of pupae parasitised by A.bilineata (Table 3.6) when presented Healthy Parasitised
Number parasitised 4.2 ± 1.0 2.4 ± 0.8 by A.bilineata
Total number attacked 4.7 ± 1.2 3.6 ± 1.3 by A.bilineata
Table 3.6 The mean number ( ± 95 per cent confidence intervals) of
healthy and parasitised (by Trybliographa rapae) pupae
attacked and parasitised by Aleochara bilineata.
There is a significant difference between the numbers
actually parasitised ( t = 3.22; p < 0.05,18 degrees of
freedom) but not between total number of pupae attacked.
Parasitised Unparasitised
Pupal weight 0.0093 ± 0.0009 0.0098 ± 0.0004 (g)
Table 3.7 The mean weight ( ± 95 per cent confidence intervals) of
both healthy and parasitised (by Aleochara bilineata)
cabbage root fly pupae. - 112 - with either 10 healthy D.radicum pupae or 10 parasitised pupae.
Although some pupae had been multiparasitised only T.rapae larvae successfully completed their development to emergence. Some pupae had obvious signs of attack by the staphylinid larvae but the para- sitoid had not entered the puparium. When such pupae were also considered there was no significant difference in the level of attack (Table 3.6).
This suggested that the staphylinid larva was determining the host's condition only after the puparial wall had been penetrated.
Previous work had shown that there was a significant size (Wishart and Monteith,1954) and weight (present study) difference between healthy
D.radicum pupae and those parasitised by T.rapae. To determine whether the staphylinid larvae discriminated on the basis of pupal size ten
A.bilineata larvae were presented with twenty, 4 - 5 day-old D.radicum pupae chosen at random from laboratory cultures. At the end of the experiment the pupae were weighed. There was no significant difference between the weight of healthy and parasitised pupae (Table 3.7).
To determine whether A.bilineata larvae actively discriminate between parasitised and unparasitised D.radicum pupae, 10 pupae of both types were presented together. The results are shown graphically in 2 Figure 3.8a. There was no significant difference (x = 10.33, p > 0.05,
19 d.f.) between the levels of parasitism by the staphylinid larvae of the two types of pupae. This was also true when pupae attacked but not 2 actually parasitised were considered (x = 8.8, p > 0.05, 19 d.f.). Of those pupae that had been multiparasitised by both T.rapae and A.bilineata, the latter parasitoid failed to emerge from any puparium. It was concluded that parasitism by A.bilineata after T.rapae reaches its ectoparasitic stage is unlikely to prove successful for the beetle as it fails to develop at a rate sufficient to usurp the cynipid larva. Bromand (1980) made a more detailed study of multiparasitism by these two parasitoids on a. 6
4
•n•nnn•••
•n•
2-
U 0 Healthy Parasitised
0. a) CO b. 6-'
.12 E 4 - =
2
0 Healthy Parasitised
Figure 3.8 The mean number ( ± 95 per cent confidence
intervals) of healthy and previously parasitised
(by Trybliographa rapae) cabbage root fly pupae
attacked (CD) and parasitised (MM) by Aleochara
bilineata larvae.
a.) Trybliographa rapae in its ectoparasitic stage.
b.) Trybliographa rapae in its endoparasitic stage. Healthy Parasitised
Number parasitised 4.2 ± 1.0 3.2 ± 0.8 by A.bilineata
Total number attacked 4.7 ± 1.2 3.5 ± 0.7 A.bilineata
Table 3.8 The mean number ( ± 95 per cent confidence intervals) of
healthy and parasitised (by Trybliographa rapae in its
endoparasitic stage) pupae attacked and parasitised by
Aleochara bilineata larvae. - 115-
D.floralis and found that approximately 46 per cent of pupae previously parasitised by T.rapae were parasitised by A.bilineata while 81 per cent of healthy pupae were parasitised. He commented that some degree of selection occurred but was unable to determine how A.bilineata larvae detected the presence of T.rapae within the puparium.
Determining whether a pupa was parasitised while T.rapae was in its endoparasitic stage proved difficult. Measurement of pupal weight had, as mentioned in Chapter 2, shown a marked difference between healthy pupae and those parasitised by T.rapae. Using weight as the means of measurement, pupae were classified as being either parasitised (1 0.0095g) or unparasitised (> 0.0095 g). As a control, 10 groups of 10 pupae believed to be parasitised by the cynipid were allowed to develop.
Trybliographa rapae adults emerged from between 70 - 80 per cent of the pupae. Classifying pupae on the basis of their weights was, therefore, considered an acceptable, although not ideal, means of determining pupal condition. However, when considering any results from observations where this method of classifying has been employed it must be realised that there is a possibility that a pupa had not, in fact, been parasitised by
T.rapae.
The same experimental procedure as that described above for the ectoparasitic stage was employed. When 10 beetle larvae were provided with 10 pupae thought to contain the cynipid, endoparasitic stage, parasitism occurred to a level similar to that when 10 healthy D.radicum pupae were presented on their own (Table 3.8). In cases of apparent multiparasitism it was A.bilineata that emerged and not T.rapae, although a considerable number of pupae did not yield either insect. Similar observations were made when 10 A.bilineata larvae were presented with a mixture of 10 healthy and 10 parasitised (by the endoparasitic stage) cabbage root fly pupae. The results are presented in Figure 3.8b. No preference was shown for either type of pupae. - 116 -
An interesting consequence of multiparasitism was the apparent increase in mortality levels when A.bilineata attacked a pupa containing
T.rapae in its endoparasitic stage. Only approximately 10 per cent of those multiparasitised gave rise to A.baineata adults, the remaining multiparasitised pupae yielding no adult insects. Although no A.bilineata emerged from the puparia containing the ectoparasitic cynipid stage approxi- mately 50 per cent of the multiparasitised pupae gave rise to adult T.rapae.
Whether multiparasitism during T.rapae's endoparasitic stage is more likely to result in neither parsitoid obtaining sufficient nutrient to complete development is unknown. Levels of superparasitism were negligible in all observations.
Multiparasitism has received relatively little consideration in the literature. Schroeder (1974) while studying the internal parasitoids of the European Pine Shoot Moth, Rhyacionia buoliana (Schiff.) (Lepidoptera:
Olethreytidae), found that, for a particular interactive complex of six species of parasitoids, interspecific competition occurred in the form of direct physical attack between the first instar larvae. Weseloh (1979) found that in the laboratory Eurytoma verticillata (F.) (Hymenoptera:
Eurytomidae), a hyperparasitoid of the Gypsy Moth, Lymantria dispar (L.)
(Lepidoptera:Lymantriidae), consistently destroyed larvae of another hyperparasitoid, Celia tenellis (Say.) (Hymenoptera:Ichneumonidae), when both were associated with the same host, Apanteles melanoscelus (Ratzeburg)
(Hymenoptera:Braconidae). Finally, van Strien-van Liempt (1983) while investigating the competition between Asobara tabida (Nees) (Hymenoptera:
Braconidae) and the cynipid Leptopilina heterotoma found that in multi- parasitised hosts, one of the two parasitoids was eliminated within a few days after the larvae had hatched. The survivor then had at its disposal the whole food supply - an example of contest competition. van Strien-van
Liempt found that both parasitoids had the same chance of surviving in multiparasitised hosts but that the outcome was dependent on the interval between the times of oviposition, environmental temperature and host stage. - 117-
The results presented above support the observation made by
Wishart and Monteith (1954) that A.bilineata hatch if the larva enters
the puparium before the T.rapae larva changes from its endoparasitic to
its ectoparasitic stage. There does not appear to be any selective
discrimination by A.bilineata for either host 'type' when presented
together but, in the light of Bromand's (1980) findings on D.floralis,
a more detailed study is required before any sound conclusions may be
reached.
3.6 Conclusions.
The prevalance of Bolling's Type 3, or sigmoid, functional response
in the present system lends further support to the belief that sigmoid
responses are not restricted to vertebrate predators. Searching effi-
ciency was believed to be directly proportional to host density, this
possibly being the result of a combination of the increased rate of
encounter with potential hosts and the increased olfactory stimulus
emanating from areas of high host densities. Different plant habitats
did not affect the functional response as much as different host
instars, third instars giving rise to a longer handling time and lower
searching efficiency. Functional response curves of the Type 3 form have
a stabilising potential but their occurrence and significance in the field
siutation remains unestablished. When two equally acceptable host popu-
lations (first and second instars) were presented together, the parasitoid
showed no active selection for either. When either first or second instars were presented together with third instars there was a marked preference for the former. Superparasitism was avoided to a considerable degree with a very high level of discrimination being shown against hosts already parasitised. There was some evidence that conspecifics could not dis- criminate other females' eggs as well as their own in the immediate period - 118 - subsequent to the oviposition of the first egg. Multiparasitism does occur, A.bilineata usurping the cynipid only if the staphylinid larva enters the puparium before T.rapae changes from its endoparasitic to its ectoparasitic stage. Parasitoid mortality increased as a consequence of multiparasitism but no evidence could be found of A.bilineata reject- ing hosts already parasitised by 1%rapae. - 119 -
CHAPTER 4
THE EFFECTS OF HOST HETEROGENEITY AND
PARASITOID DENSITY ON PATTERNS OF PARASITISM
The various forms of the functional response considered in the previous Chapter, and described as 'ecologically primitive' by
Putman and Wratten (1984), are formulated in a system where parasitoid
(or predator) individuals search at random for a fixed density of randomly arranged hosts (or prey). Under natural conditions host populations are usually distributed in a heterogeneous manner (for example, Cheke,1974; Doncaster,1981; Nachman,1981; Hildrew and
Townsend,1982; Kidd,1982; Drake,1983), tending to aggregate in areas of favourable food or microclimate conditions. Consequently, an efficient parasitoid (or predator) should spend more time and lay more eggs (or consume more prey) in areas of high host (prey) density than in regions where resources are limited. Numerous examples are provided in the literature of foraging animals aggregating and spend- ing more time in areas where resources are plentiful (for example,
Goss Custard,1970; Akinlosotu,1973; Collins, Ward and Dixon,1981; van Alphen and Galis,1983). Such a response is often referred to as the 'aggregative response'.
This Chapter sets out to explore the pattern of parasitism shown by T.rapae when presented with a heterogeneous environment with patches in which different numbers of host larvae are present. From the data collected and by making similar studies in the field, in as natural an environment as experimental procedure will permit, it is hoped to establish the relevance of laboratory observations to what happens under natural conditions. This latter objective will be con- sidered in Chapter 5. Section 4.1 below provides a short introduction - 120- to the considerable amount of work available on the effect of habitat heterogeneity on host-parasitoid population dynamics and aims to provide a suitable background on which later discussions will be based.
4.1 Introduction.
4.1.1 Host Heterogeneity.
When considering host heterogeneity, it is common to describe the
environment as being composed of a number of patches of high and low
densities of the organism being attacked. It is important to define
what a patch actually is. Past studies show considerable variation in
what the experimenter has assumed, somewhat arbitrarily, constitutes a
patch. Akinlosotu (1973), for example, while exploring the aggregative
response of a parasitoid, Diaeretiella rapae (Curtis.) (Hymenoptera:
Braconidae), of the cabbage aphid, Brevicoryne brassicae (L.) (Homoptera:
Aphididae), considered a patch to be single leaf. Hubbard (1977), on
the other hand, while studying the response of the braconid Apanteles
glomeratus (L.) to Brassica plants inoculated with different densities
of Pieris brassicae (L.) (Lepidoptera:Pieridae), applied the term
patch to the whole plant. Royama (1971b.) took this further by stressing
that from the parasitoid's point of view it was not the density of hosts
in a given patch that was important, but rather the actual number of
hosts each parasitoid could attack within a given time period in a
given area. He defined his patches, or hunting stations, in terms of
profitability that was not linearly related to the density of hosts.
Hassell and Southwood (1978) have argued for the existence of a
hierarchy of patchiness (described in Chapter 2) and Waage (1977) has
stressed the importance of not identifying patches solely by what the
observer perceives and considers reasonable. A patch should, instead,
be defined by the forager as an area which contains a stimulus (or - 121 - stimuli) that, at the proper intensity, elicits a characteristic foraging activity in a responsive forager. Taking this and the observations made during the olfactory studies described in Chapter 2 into consideration, in the following experiments a 'patch' has been taken to be represented by a disc of swede in which a specific number of cabbage root fly larvae were burrowing.
From the numerous studies made of the foraging behaviour of both parasitoids and predators (for examples see Hassell, 1978), considerable interest has been directed towards establishing how the foraging time is allocated between patches of different profitability. This interest has, in general, been divided into two groups, those showing that certain patterns of foraging may increase population stability (for example, Royama,1971b.; Hassell and May,1973,1974; Murdoch and Oaten,
1975) and those concerned with describing behavioural adaptations which maximise the effects of foraging (for example, Charnov,1976; Cook and
Hubbard,1977; Comins and Hasse11,1979; Waage,1979; Anderson,1984).
Krebs (1978), Hassell and Southwood (1978), Pyke, Pulliam and
Charnov (1977), Cowie and Krebs (1979) and Krebs and McCleery (1984) have all reviewed the optimisation of foraging behaviour and the various models will not be considered in the present context. Of considerable importance is the way in which patch time is allocated and what criteria are adopted for leaving a patch. Waage (1977) suggests four different behavioural mechanisms that could be involved in the determination of the duration of a patch visit. These four mechanisms lead to very different aggregative responses (Figure 4.1):
(1.) Fixed number mechanisms. This is the 'hunting by expectation'
hypothesis of Gibb (1962), the forager leaving the patch after
a fixed number of prey have been captured. a. b.
c.
•Vcs
Th in 0
Host density per patch.
Figure 4.1 Hypothetical relationships between the time spent by a
parasitoid in a patch and the host density per patch.
(a.) A fixed number of hosts are parasitised in a patch
before leaving. (b.) A fixed amount of time is spent
in a patch before leaving. (c.) A fixed amount of
searching time is spent before leaving (valid only if
finite handling time is considered). (d.) The parasitoid
leaves a patch when the rate of host attack falls below a
fixed level. (after Waage, 1977) - 123-
(2.) Fixed time mechanisms. The 'hunting by time expectation'
hypothesis of Krebs (1973) where the forager leaves after
a fixed amount of time has been spent in a patch.
(3.) Fixed searching time mechanisms. The forager leaves after a
constant searching time per patch.
(4.) Fixed rate mechanisms. The forager leaves when the rate
at which the resource is encountered falls below a fixed
threshold.
Hassell and May (1974) and Murdoch and Oaten (1975) assume this threshold capture rate to be constant. Charnov (1976), on the other hand, assumes that the 'giving-up threshold' depends upon the average resource density within that particular habitat. Parasitoids should, as a result, tend to reduce all patches to the same 'marginal value', the parasitoid's expected rate of attack for that particular habitat.
The majority of studies on foraging behaviour have been restricted to laboratory systems. As Waage (1983) states, little is known of how parasitoids forage in the field as much of our understanding of para- sitoid foraging in nature is based largely on inference from field patterns of parasitism. The only means of properly assessing natural patterns of time allocation and their consequences is by direct field observations of foraging parasitoids. Observing T.rapae in the field proved difficult and unrewarding. However, by making detailed observa- tions of the foraging behaviour of the cynipid parasitoid in the laboratory (this Chapter) and comparing and contrasting the resulting patterns of parasitism under both field (Chapter 5) and laboratory conditions, it was hoped to be able to relate the patterns of foraging, and resulting levels of parasitism, that occurred in both environments.
The aggregation of parasitoids where hosts are abundant provides a potentially powerful stabilising mechanism for host-parasitoid - 124-
interactions (Hassell and May, 1973). Hassell and May found that
this stability, increasing as a result of the relative protection
afforded to the host individuals found in the low density patches,
was dependent on four factors: the level of parasitoid aggregation,
the host's rate of increase, the proportion of the host population
in the high density patch and the number of low host density patches.
The importance of this last factor was further supported by Maynard
Smith (1974) who found that stability was enhanced by increasing the
number of spatial sub-units.
A number of population models describing such aggregative behaviour
(for example see that of Hassell and May (1973) above) assume the para-
sitoid to have a fixed aggregation strategy. This leads to over- aggregation, particularly at high parasitoid densities, with the parasitoids remaining at high host densities even when most of the hosts have been attacked. As a consequence of over-exploitation, the instantaneous search rate, a', is lowered and, as Hassell (1978)
illustrates (Figure 4.2), random search would have fared better. Real parasitoids would not have shown such 'irrational persistence' but would have abandoned the patches to seek more profitable areas elsewhere.
Royama (1971b.), in particular, considers profitability of a hunting
station as one of the most important considerations for a foraging parasitoid. Profitability can be defined as the number of hosts a parasitoid can parasitise in a given time in a given area. If a strong aggregative response is a feature of the interaction, increases in the number of parasitoids on stations or patches of high host densities may lower the profitability of that station. To forage optimally therefore involves the movement of searching individuals to other patches to ensure that maximum profitability is achieved. By making detailed observations of how searching time was allocated to various patches with differing host numbers, the studies described below attempt to explore Clumped search.
.0 0 Random search. eti m 0 oT o -J
Log ic) parasitoid density.
Figure 4.2 A schematic picture to illustrate both the increased
searching efficiency at low and intermediate parasitoid
densities and the apparent interference relationships
that arise from parasitoids always aggregating in patches
of high initial host density rather than searching at
random. The broken line illustrates a more prudent para-
sitoid strategy in which aggregation gives way to random
search at high parasitoid densities. (from Hassell, 1978) - 126- how the movement of T.rapae over the arena, and the way in which it exploited patches, was affected by the number of foraging parasitoids.
Other models have been developed which are more complex. By using the negative binomial distribution, Hassell and May (1974), for example, included easily measurable parameters that characterise parasitoid aggre- gative responses to realistic host distributions. This more detailed model supports the findings of the simpler model described above,
stability being enhanced by increased prey clumping and marked predator
aggregation. Hassell (1978) does, however, state that in making these
models of aggregation more complicated in an effort to capture some
essential components of parasitoid and host distributions, such com-
plexity 'leads rapidly to analytically intractable models which are a
deterrent against further elaboration of the systems'.
4.1.2 Pa ra sitoid density.
As foraging animals show this tendency to aggregate and spend more
time in patches where resources are more plentiful, they are more likely
to come into contact with one another and, in the case of parasitoids,
with previously parasitised hosts. The likelihood of encounter
increases the higher the density of the forager. These encounters
have been classified by Hassell (1978) as mutual interference and such
interactions can lead to an increased tendency to disperse (for example,
Akinlosotu,1973; Noyes,1974) and an increase in the number of non-
foraging individuals (Rogers and Hubbard,1974). This may result in
marked changes in the number and distribution of parasitoid progeny.
It was Hassell and Varley (1969) who proposed that searching
efficiency, as measured by the Nicholsonian (1933) area of discovery,
a, did not remain constant with varying parasitoid densities but that - 127 -
it declined at a constant rate m, the mutual interference constant or the coefficient of interference.
By substituting a = a'T in Equation 3.3, searching efficiency, a, may be defined by N 1 a = a'T = — t 4.1 P log e[ N - N J. t t a
If a remains constant, Equation 4.1 provides the mathematical basis for
Nicholson's (1933) classic competition curve. Assuming a linear relation- ship on logarithmic scale between searching efficiency, a, and parasitoid density, Pt,
log10 a = log10 Q - m log10 Pt 4.2 or a = Q Pt-m • 4.3
Here log10 Q, the intercept, is the value of log 10 a when the logarithm of parasitoid density is equal to zero. On this basis the Nicholson-
Bailey model can be modified to
1-m N =AN [ -QPt 4.4 t+1
P t+1 Nt [ 1 - exp (- Ptin ] . 4.5
Such a modification has a marked effect on the model's stability.
By increasing the value of the mutual interference constant Hassell and
Varley (1969) found a greater tendency for the host-parasitoid model
to stabilise. The interaction is made more unstable as m approaches
zero and, when in = 0, efficiency is not affected by changes in para-
sitoid density, the model reverting to the original Nicholson-Bailey
system. Hasse/1 and May (1973) analysed the stability properties of the model further and showed conclusively that given suitable values for both
the interference constant and the prey rate of increase, A, a stable
equilibrium is possible. The third parameter, Q, only affects the
equilibrium levels of the populations and has no effect on their
stability. - 128-
Hassell and Varley's (1969) simple model of mutual interference
is, however, somewhat unrealistic in that, as Royama (1971a.), Rogers
and Hassell (1974) and Beddington (1975) have all mentioned, searching
efficiency can not continue to rise indefinitely as parasitoids become
increasingly scarce. It is more likely that searching efficiency will
tend to level off at low parasitoid densities when interference is
negligible (Figure 4.2). The presence of behavioural interference in
the laboratory does not necessarily imply that it is an important factor
in natural host-parasitoid interactions. The scarcity of comparable data
from both field and laboratory studies has, however, made establishing
the relevance of laboratory work to the natural situation difficult.
In the experiments that follow the levels of interference occurring
under the described laboratory conditions are established. These will
then be compared, in Chapter 5, with the degree of interference recorded
in the field from comparable observations.
Hassell (1982a.) attempted to define searching efficiency within
the context of population models and a patchily distributed host popu-
lation. Holling's (1959b.) model assumes that exploitation of hosts
(or prey) during the interaction time is minimal, no discrimination being show by the parasitoid against hosts already parasitised, and prey being replenished as eaten. Numerous workers (e.g. Nicholson,
1933; Nicholson and Bailey,1935; Royama,1971a.; Rogers,1972) have incorporated host depletion in their host-parasitoid models by assuming that the host individuals are encountered at random. The number of hosts attacked is then given by Equation 3.6, from which the instantaneous search rate, a', may be calculated. Such a definition is applicable to homogeneous host populations which are randomly exploited by para- sitoids but, as has already been mentioned, hosts, in most cases, are patchily distributed. - 129-
Hassell (1978,1982a.) argued that in such heterogeneous situations
searching efficiency must be considered at two different levels, that within a single patch and that over all the patches. If exploitation within a patch is random, then the patch specific searching efficiency will be given by
N 1 a / - 6 [ ] 4. P . T e N - N ' i si ai where i is a specific patch. An overall measure of searching efficiency
in the environment can be determined by considering the values of a' for
the different patches sampled. If the distribution of hosts, parasitoids,
searching time and hosts attacked over a number of individual patches, n, is known then an overall searching efficiency can be obtained from
n N. 1 E r 1 7, a , = n log [ I. P. T e N. - N i=1 1 si 1 ai
This can be considered as being the average of the searching efficiency values obtained for each patch and, as Hassell (1982a.) states, although labour intensive, by taking account of both the actual searching time per patch and the resulting number of hosts attacked, it provides the most accurate measure of real searching efficiency within a patchy environment. In the present study this more detailed estimation of searching efficiency was applied in the laboratory where parasitoids could be continuously observed. Under natural conditions, where such continuous observation was not practical, searching efficiency was estimated using the simpler Hassell and Varley (1969) model, Equation
4.1.
Care must be taken in ascribing the reduction of searching effi- ciency as parasitoid density increases entirely to the behavioural effects of mutual encounters. Free, Beddington and Lawton (1977) comment that by concentrating on profitable patches a single parasitoid does, indeed, increase the number of hosts it attacks per unit time - 130 -
from what it would attack if foraging randomly. However, by removing hosts from these profitable patches, there will be a reduction in the patches' profitability. Consequently, aggregated search will approach random search and the efficiency of the parasitoid will decrease.
Clearly, this decrease will be far more obvious and immediate if there are many parasitoids. Thus, attack efficiency appears, as a consequence
of aggregated behaviour, to decrease as parasitoid density increases.
This is known as 'pseudo-interference'.
Hassell (1971,1978) illustrates very clearly how important this pseudo-interference can be. By exposing various densities of the larvae of the flour moth, Ephestia cautella, to differing numbers of the para-
sitoid V.canescens, he showed that 33 per cent of the total interference observed was accounted for by parasitoids leaving host patches. A further 27 per cent was explained by the parasitoids being interrupted on encountering one another, leaving 40 per cent of the total unaccounted for by actual mutual interference. If the assumption of random search was abandoned and account taken of the distribution of attacks and the time spent on various patches (by using Equation 4.7) in estimating the
searching efficiency, the amount of interference remaining unexplained was insignificant. This suggested that the 40 per cent remaining was pseudo-interference, attributable to the aggregated behaviour of the parasitoid.
*******
In Experiments 4.1 and 4.2 below the allocation of foraging time
to various host densities is explored, as is the effect of increasing
the number of active foragers in the environment. From these obser- vations the searching efficiency of the parasitoid is considered and
the levels of intra-specific interactions determined. These observations
are then considered in the light of the results of a third experiment
(Experiment 4.3) where the effect of using a homogeneous, uniform dis-
tribution of hosts on levels of parasitism is investigated. - 131 -
4.2. Experiment 4.1 : To determine the effect of a heterogeneous
host environment on the levels of parasitism
reached by a single Trybliographa rapae female.
4.2.1 Materials and Methods.
Standardised (i.e. 0-2 day-old) adult female T.rapae were allowed to oviposit in second instar hosts for 12 hours prior to experimental use to gain experience. Swede discs of the same dimensions as those described earlier (Chapter 2) were cut and 2,4,8,16 or 32 second instar cabbage root fly larvae were allowed to burrow into the plant tissues
24 hours prior to the start of an experiment. This allowed sufficient time for the larvae to penetrate the swede and to start producing frass which, as was shown in Chapter 2, acts as an attractant to the parasitoids.
Five discs, with differing host densities, were arranged in a pen- tagon in the centre of a plastic arena measuring 45 cm x 45 cm x 10 cm
(see Figure 4.3), with the floor covered in approximately 0.5 cm of dry, washed sand. A single, experienced female was placed in the arena and
the time spent on each patch, a swede disc, observed and recorded on a
Rustrack 8-channel event recorder for 8 hours. The experiment was
repeated five times. At the end of this period the wasp and swede discs
were removed. After a further period of 24 hours the swede discs were
cut open, the larvae removed and dissected to determine the number of
hosts parasitised in each patch and to check for any superparasitism.
Analysis of the event recorder chart enabled both the time of consecu-
tive patch visits and the total time spent on each patch over the eight-
hour period to be determined. a.
swede sand disc
b.
swede disc 00
Figure 4.3 Arena used for observing the response of Trybliographa
rapae in a heterogeneous environment, (a.) cross-
section of arena, (b.) position of swede discs in arena. - 133-
11.2.2 Results and Discussion.
Time spent on a patch was defined as the time between a female
alighting on and leaving a patch. The total time spent on a patch is
composed of a number of categories such as time spent searching, handling time, time wasted when hosts are rejected and time spent
doing other activities such as cleaning and resting. The proportion of time spent on these latter activities was negligible and has not been considered in the analyses. As mentioned previously, observing
an actual oviposition was difficult in the present experimental design as neither could the larval hosts be seen nor was it possible to deter- mine from the parasitoid's behaviour whether or not oviposition had actually taken place. Handling time is believed to be short relative
to the time taken to locate potential hosts, the host being paralysed prior to oviposition (L.Vet,pers.comm.).
As Figure 4.4 illustrates, the total time spent on a patch increased
in a curvilinear manner with increasing density of host larvae. An
increased encounter rate with potential hosts on the high density patches could have resulted in such a pattern, encounters with hosts prolonging the time spent actively foraging in these areas. There may also have been an incremental effect on the relative searching times as a result of the higher concentration of larval by-products on these patches or, indeed, a combination of both factors.
Waage (1977) explored whether the ichneumonid parasitoid V.canescens acted selectively in the way in which it exploited host patches. He suggested that this selectivity could arise from differential attraction to patches of different density and/or preferences developed for certain patches as a result of experience. The order in which the different host areas were exploited by the 5 females is given in Table 4.1. From the limited data available (Table 4.2), the order in which first and 0.5-
0-0
No. hosts in patch, N t .
Figure 4.4 The time spent by a single female parasitoid on
patches of various host densities. — 135 —
VD N N .•,.. C•"1 efl
if) N N .-- c•-1
N
cril ...i. co
N N %,0 ,--
.- N N N N .-• cr) Cr) cr) cr)
0 N N (s. kO .- (r) frl Cr) .--
01 N CO N CV Cr) Or) VI
00 N ..1* N ‘,C) Cr) Cr) .--
N. csi n10 n0 ..." N .- .- CI) Cr) • •O 0 -ri %.0 N CO N N k0 I-4 VI el Crl .-- C) 0.
Iv) C•1 %.0 N CO CO Cr) ...- Cr)
-Zr n0 N V::. -4 N •n-• Cr) .n-• cr)
Cr) N N CO N *.f, Cr) r) el ..-
k0 N N CO -Zr N v1 cr)
.-- CO N -4 CO N cr)
— c., cf, ,i. in ds em Number of Visit number hosts in patch 1st 2nd 3rd 4th 5th 6th 7th
32 1 2 3 2 2 3 2
16 0 1 1 2 1 1 2
8 2 1 1 0 2 1 0
4 1 1 0 1 0 0 1
2 1 0 0 0 0 0 0
Table 4.2 The allocation of successive visits to five patches
of various host densities. Results obtained from
observations made on five female wasps. - 137-
subsequent patches were selected did not show any non-random selection.
As a consequence of the small number of replicates the results do not lend themselves to any meaningful statistical test and it can only be
suggested that the wasps were attempting to explore the arena, testing each patch individually. This would be in marked contrast to the optimal foraging model described by Royama (1971b.) where high host patch densi- ties are exploited initially followed by sequential steps to the lowest patch densities.
That the wasps did initially search the arena in an exploratory fashion is illustrated very clearly when the eight-hour period is divided into hourly sections (Figure 4.5). By plotting the time spent on each patch, as a proportion of the total time spent on the patches during that hour, against both the number of hosts and the hours since the experiment began, any changes in the way that patches of different densities were being exploited may be investigated. During the initial period all five patches were explored by the parasitoid and from the very large confidence intervals it is obvious that there was no real difference between the times spent on the different areas. As the experiment progressed there was a narked change in the pattern of attacks. The wasp showed a marked preference for the high host density patch and there was a reduction in the variation between replicates. Indeed, over the last 60 minutes of the experiment all the time spent on potential host areas was spent on this one patch.
Whether experience of a particular patch affects the subsequent selection of other patches can not be justifiably explored in any detail using the present data. By classifying the available data, presented in Table 4.3, into two groups (patches containing eight or fewer hosts and those containing more than eight potential hosts) it was found that the wasps did not show any significant tendency (Fisher exact test, 1.0
0.9- MEW
08-
=Oa
0 .7-
.0 4.) Ta el a a. o
=M.
a. in 0 . 4 -
0. 0.3-
0.2-
0 . 1 -
0.0 1 2 Hours 3 from start of observation. z
824 8 16 32 Hosts per patch, N t .
Figure 4•5 Patch-time allocation of a single foraging parasitoid
at hourly intervals during the eight hour observation
period. Results obtained from observations on five
females; mean ± 95 per cent confidence intervals are
given. - 139-
Patch coming from
2 4 8 16 32
2 0 0 0 0 2
4 0 0 3 2 1
8 0 1 1 4 3
16 0 1 2 0 9
32 1 3 1 6 17
Table 4.3 Table to investigate the effect of previous experience
on patches and whether this affects subsequent patch
choice. 80- 32 60-
40-
20
0
60- 16 40-
20-
0
40- 8 20-
0
40- 4 20 -
0-
20 -Li 2
0 1 2 3 4 5 6 7 8 No. of patch visit.
Figure 4.6 Average time spent in successive visits to one patch,
with 95 percent confidence intervals, for differing
initial patch densities. A 60 second criteria was
used for patch leaving. - 141 - p = 0.87) to select either group of patches for subsequent visits on the basis of experience gained from any previously encountered patch. It is, however, doubtful whether this may be considered conclusive evidence for
the lack of learning by experience in T.rapae.
Previous foraging on patches with host densities between 4 and 16 had a significant effect on the duration of successive patch visits
(Figure 4.6). For the patch with 32 host larvae, previous experience of the patch did not appear to have any effect on the duration of return visits. An increased encounter rate with hosts parasitised during the first visit on the low density patches does not explain the pattern as hosts were not parasitised on these patches. There are two other possible hypotheses. Firstly, that during the initial visit the substrate was marked chemically by the ovipositor while probing. If this marker func-
tioned as some form of deterrent, the duration of any subsequent visit could have been determined by a combination of the shortening effects of
the marker and the increased responsiveness arising as a result of the chemical stimuli emanating from the patch. This latter factor would have been strongest on the high density patch.
Secondly, it may be assumed that a wasp on a high density patch
searched a smaller area than one on a patch of lower density. If the wasp did mark the substrate while probing it may be further assumed that on the low density patches most of the disc area was searched and marked during the first visit. If the marker deters further searching, a second visit would have ended as soon as contact was made with the chemical marker. On a high density patch, where a smaller area was searched, the wasp could return to the same disc and find an area not previously
searched and hence unmarked. If the area searched varied with host den-
sity it would be expected that second visits would have lasted longer
the higher the density of host larvae. The strong correlation between • •
• / II r I 1 24 8 16 32 No. hosts in patch, Nt.
Figure 4•7 The relationship between the ratio of the second to
the first visit on a single patch and the number of
hosts present on that patch. - 143-
the ratio of the second to first visits and the host density
supported this expectation (Figure 4.7).
The use of marker substances by parasitoids, in particular to
ensure avoidance of superparasitism, has been well documented for
numerous species. van Lenteren (1976) made a survey of 21 different
species showing such behaviour, the majority marking the host itself
both externally and internally. Greany and Oatman (1972), however,
in a study of Orgilus Zepidus (Musebeck) (Hymenoptera:Braconidae),
a parasitoid of the potato tuberworm, Phthorimaea operculella (Zeller)
(Lepidoptera:Gelechiidae), found that the host medium was marked by
grooming a substance produced in the Dufour's gland of the ovipositor
onto the medium immediately after oviposition. More recently, Harrison,
Fisher and Ross (1985) have suggested that V.canescens may deposit an
external marker, again from the Dufour's gland, in the host's vicinity
preceeding, during or after oviposition. Similarly, Sugimoto, Uenisi
and Machida (unpublished manuscript) found that the braconid
Daspilarthra rufiventris (Nees.) discriminated against searching leaves
of Ranunculus glaber (Makino) already explored by itself or conspecifics.
Such behaviour was found to arise from the presence of a substrate mark deposited by the parasitoid while probing. Daspilarthra rufiventris not only marked the leaf mines containing the hosts, larvae of Phytomyza ranunculi (Schrank) (Diptera:Agromyzidae), but all the leaf surface explored while searching for potential hosts. Other parasitic insects, for example, the alfalfa blotch leafminer, Agromyza frontella (Rondani)
(Diptera:Agromyzidae) (McNeil and Quiring, 1983), are also known to mark the substrate with an oviposition-deterring pheromone after oviposition.
Such substrate marks may play an important role in avoiding repeated search on a limited site, preventing the wastage of both the parasitoid's time and energy reserves. - 144 -
4•3 Experiment 4.2: To determine the effect of parasitoid
density on the pattern of parasitism of
Delia radicum by Trybliographa rapae.
4.3.1 Materials and Methods.
Host instars were standardised as for Experiment 4.1 and arranged
in the arena in a similar pattern to that already described. Stan-
dardised wasps were introduced into the arena in numbers ranging from
five to twenty and by careful observation the parasitoid-hours spent
on each of the five patches were noted using the event recorder. In
addition, any interactions occurring between the wasps were observed
and the time wasted as a result of such interactions recorded. (As
will be discussed below, this period of time was negligible, the presence
of another wasp in the near vicinity not appearing to influence unduly a
foraging parasitoid's behaviour.) Results were collected and analysed
as in the first experiment.
4.3.2 Results and Discussion.
Experiment 4.1 established that T.rapae exhibited a marked aggre- gative response, spending significantly more of its foraging time on patches of high host density. This experiment enabled the effect of the increased likelihood of encounters between parasitoids on areas of high host density to be established. The results are presented graphi- cally in Figure 4.8.
There was a marked tendency at all parasitoid densities for the female wasps to aggregate in patches of high host density. This gave rise to directly density dependent responses where a higher percentage of hosts were parasitised on the more densely populated patches. As parasitoid density increased, lover host density patches were exploited to a greater degree with resulting higher levels of parasitism than at Figure 4.8 (a.) The aggregative response of Trybliographarapae in
terms of proportion of total observed time spent by
adult parasitoids on patches of different densities,
with parasitoid density ranging from 1 to 20.
(b.) The same experiment but shown in terms of
percentage parasitism. a.
0-5- E
}
0-0 32 h N t. 16 J:. I 1 1 ) 2 1 ; 10 15 20
Pt.
50-
40 -
30 -
20 -
10 -
*NIP
32 No. of hosts 16 per patch, Nt.
2i 5 10 No. of searching parasitoids,P t . -2-0- • ••• •••n • 2 0 •
O.. • CO
0
0 -25-
-3-0
0 1 2 Loge P t .
Figure 4.9 The change in searching efficiency, a', estimated
from Equation 4.1, with increasing parasitoid densities.
Solid line gives linear regression (equation of line is
given by y = -2.02 - 0.39x; r = 0.78, p < 0.001);
broken line fitted by eye. - 148- low parasitoid densities (Figure 4.8b.). This higher level of exploitation of the low density patches when more parasitoids were foraging is likely to have been the result of a combination of behavioural interactions between individuals on the high density patches and an increased encounter rate by individual females of previously parasitised hosts on these patches.
Searching efficiency, a', may be calculated from Equation 4.1.
When plotted on a logarithmic scale against parasitoid density a significant linear relationship was found to exist (Figure 4.9), log10 Q and m being estimated from the intercept and slope of the plot, respectively. However, by observation it is obvious that the best fitting relationship is not linear but markedly curvilinear (Figure 4.9), with searching efficiency levelling off at the lowest parasitoid densi- ties. As described in Section 4.1, Beddington (1975) and Free, Bedding- ton and Lawton (1977) comment on the likelihood of searching efficiencies tending to level off at low parasitoid densities where interference is negligible. Hassell (1978) provides examples from the literature which show the prevalence of such a response form and suggests that where linear relationships provide suitable descriptions, they may, in fact, be representing linear approximations to the whole or, more likely, segments of the curvilinear response.
As mentioned earlier, any measurement of the mutual interference constant, m, incorporates both mutual parasitoid interference and aggregation or pseudo-interference. Although not always the most accurate description of the relationship between searching efficiency and parasitoid density, the linear model does enable the level of inter- ference to be explored and analysed in similar detail to that of Hassell
(1971,1978). From the results collected during the observations of
T.rapae foraging, estimates were made of the total time spent by the parasitoid searching on swede discs, the time spent by each parasitoid - 149- on each individual swede disc and the time wasted when two parasitoids encountered one another. Figure 4.10 illustrates how interference may be analysed on the basis of these time estimates.
The first line in the figure, A, is the all-inclusive interference relationship described previously and is based on Equation 4.1. In this case the results were summed over all 5 patches, the interaction time, I', was taken to be the total duration of the experiment, 8 hours,
N was the total host density (62) and N was the total number of hosts t a parasitised. Using these values, m was estimated to be 0.39.
The average time spent by a T.rapae individual on the swede discs was expected to decrease as the parasitoid density within the experimen- tal arena increased. This would have arisen as a consequence of mutual interference causing the parasitoids to leave patches containing potential hosts and thus spend less time searching. To allow this to be taken into account, the total observation time of 8 hours was replaced with the actual time spent foraging on areas containing potential hosts. The apparent searching efficiency at the higher parasitoid densities in- creased slightly and yielded line B (m = 0.36). This, however, only explained some 8 per cent of the total observed phenomenon. This was not entirely unexpected since, as Figure 4.11 illustrates, there was little change in the time spent by an individual female parasitoid on the swede discs as the number of foragers increased. Some other factors still applied.
The number of actual encounters that resulted in the female wasp changing its behaviour in any way that affected its foraging was also negligible. It was frequently observed that an actively probing female wasp was not influenced unduly by another female parasitoid even when the latter walked across its path. This is taken into account in Line
C (m = 0.35) of Figure 4.10, time wasted as a result of such inter- -15 -
1 0 1 2 Log io parasitoid density.
Figure 4.10 Relationships between the search rate, a', and the
density of searching Trybliographa rapae. (For clarity
individual results have not been included.) The difference
between slopes A and C is explained by behavioural inter-
ference and that between C and D by pseudo-interference. 1-0 -
• 0 -8 - • • • • • .2 0-6 -I .2 • • • • 0-4 - •
0 -2 -
0 10 20 Pares Hold density.
Figure 4.11 The relationship between the proportion of time spent
by an individual parasitoid on a swede disc and the
density of Trybliographa rapae within the experimental
arena. - 152 -
actions having been included in the calculations. The difference
between searching efficiencies when total time spent on a patch was
used (Line B) and when time wasted as a result of encounters between
parasitoids was subtracted (Line C) was negligible. Interruption of
searching by parasitoid encounters described only a further 3 per cent
of the total interference level.
Even after subtracting the effect of behavioural interference
89 per cent of the total interference observed still remained un-
explained. As described above, such non-random parasitism as observed
in this study can give rise to pseudo-interference (Free, Beddington
and Lawton, 1977). By applying Equation 4.7 and taking each patch
into consideration, the level of pseudo-interference was determined
(Line D, m = 0.24). However, even the sum of mutual and pseudo-
interference did not account for all the interference observed.
Mutual interference was the cause of 11 per cent of the total, pseudo-
interference explaining a further 28 per cent. This left 61 per cent
of the total interference remaining unexplained.
Any attempts at explaining the remaining interference must consider
that an important factor not included in the calculations above was that
the time spent on a patch was not necessarily spent in active searching.
Assuming that there was a reduction in active foraging behaviour as the
parasitoid density increased, estimates of searching efficiency would
then be too low, the error increasing the higher the parasitoid density.
Casual observations made during the experiment suggested that this factor
did not play a major role in the interaction. As mentioned briefly in
Chapter 2, when a female parasitoid was searching, certain areas were
probed more intensively than others, even on the same patch. Equation
4.7 has taken account of the pseudo-interference that arose from the differential exploitation of the five patches. However, no attention has been given to the possibility that, within a single patch, various - 153- areas might have been exploited to different degrees. This would have given rise to intra-patch pseudo-interference in addition to the inter- patch form already accounted for and could be responsible for equalising the searching efficiencies at various parasitoid densities. It could then have been inferred that all interference had been successfully abstracted.
The breakdown of patch-time allocation for densities of five, ten, fifteen and twenty parasitoids is shown in Figure 4.12. It is useful to compare these with the division of patch-time obtained with one parasitoid (Figure 4.5). In the latter case there was negligible difference in patch-time allocation during the first few hours and considerable variation between replicates. Towards the end of the observation period there was a marked selection for the patch with the highest host density (32) with the females from all replicates spending all their searching time on this one patch.
As seen from Figure 4.12, as a result of increasing the parasitoid density, a higher proportion of searching time was allocated to patches other than the high density ones. However, even at a density of ten parasitoids an increase was still observed in the fraction of time spent on the patch containing 32 hosts as the experimental period progressed, while that spent on the lower density patches decreased.
At densities of 15 and 20 parasitoids the trend was somewhat different.
Although proportionally more time was spent on the high density patch during the first hours, there was a subsequent decrease in the time allocated to this patch as the experimental period drew to an end.
Associated with this was an overall increase in the fraction of time spent on the swede disc containing 16 hosts. Towards the end of the observations, equal periods of time were spent on the two patches with
the highest densities. In this way host areas which had been heavily Figure 4.12 The allocation of searching time (mean ± 95 per cent
confidence intervals) on patches of different host
densities over an 8 hour observation period.
(a.) Parasitoid density = 5; (b.) Parasitoid density =
10; (c.) Parasitoid density = 15; (d.) Parasitoid
density = 20. - 155 -
a. 0-9-
I • • 0-8-
0-7-
0-2-
0-1 -
0-0 1 2 3 Hours 4 from start 5 of observation 7 82 4 8 16 32 Nt. 0-9 C. 0.8-
0.7-
•
02-
0.1-
0.0 1 2 Hours 3 4 from start 5 of observation. 7 24 8 16 32 Hosts per patch. Nt. - 156 -
b. O9
0.8
0•7
=MP
OINE,
0•2
0•1
0•0 1 2 Hours 3 4 from start 5 of observation. 6 824 16 32 0 . 9 - Nt.
0. 8 - d.
0 . 7 -
OW.
0 . 2 -
0.1-
0.0 1
Hours 4 from start 5 of observation. I 824 8 16 32 Hosts per patch. N t. - 157-
Number parasitoids Number hosts Number of eggs attacked per host
1 18 1.00 ± 0.00
5 84 1.04 ± 0.04
10 96 1.14 ± 0.09
15 95 1.38 ± 0.12
20 90 1.48 ± 0.14
Table 4.4 The mean number of eggs (± 95 per cent confidence
intervals) laid per parasitised host at different
parasitoid densities. - 158- exploited were left and the wasps moved to areas where there was a higher, or at least equal, likelihood of finding suitable hosts.
Finally, in assessing the effect of increased parasitoid densities on the pattern of parasitism, consideration has to be given to the levels of superparasitism that occurred. Table 4.4 records the mean number of eggs laid per host (not including unparasitised larvae) at various parasitoid densities. There is a significant difference between the means (ANOVA, F = 21.48, p < 0.01). Within the eight hour period over which observations were made, the more dense populations of aggregating parasitoids showed a higher tendency to superparasitise.
This could simply have been the result of a reduction in the rate at which parasitoids were encountering unparasitised hosts. If, however, conspecific females were unable to recognise hosts parasitised by other females, as results already considered suggest (Chapter 3), then a higher number of foraging individuals would explain the higher levels of superparasitism. In fact, considering the high density of wasps in the arena, levels of superparasitism were notably low. Under field conditions, where it would be unlikely for such high numbers of foraging wasps to be found within such a small area, it is unlikely to be of any significant consequence.
4.4. Experiment 4.3 : To determine the effect of host
distribution on the levels of parasitism
of Delia radicum by Trybliographa rapae
females.
As most host populations under natural conditions exhibit a clumped distribution between units of their habitat, models such as
that of Hassell and May (1973) take into account the effect of both parasitoid (or predator) and host (or prey) distributions. Such - 159 - models are, however, built on a mainly theoretical background and the
literature provides very few examples of studies where the actual
effect of host spatial distribution has been considered.
Eveleigh and Chant (1981) found for Phytoseiulus persimais
(Athias-Henriot) (Acarina:Phytoseiidae) that the spatial distribution
of the prey, the protonymphs of Tetranychus pacificus (McGregor),
affected its searching success and functional response. Most prey
were killed by P.persimilis when they (the prey) were clumped, followed
by random and uniform distributions. In a study of the effect of
increased clumping of pupae of the blowfly Calliphora vomitoria (L.)
(Diptera:Calliphoridae), T.H. Jones (unpublished data) found that the
chalcid parasitoid Nasonia vitripennis (Walker) did not fare as well
on the more clumped distributions. Increasing the level of host aggre-
gation resulted in fewer hosts being parasitised with the sex-ratio
changing in favour of the male. The high level of interference arising
from aggregation of the female parasitoids in areas where hosts were
plentiful and its resulting effect of increasing male production
(Wylie, 1976) were suggested as explanations for these observations.
By distributing the hosts among five patch areas, as in Experi-
ments 4.1 and 4.2, in an even, rather than aggregated, manner and
making comparable observations to those already described, the follow-
ing observations attempt to determine the effect of host aggregation
on patterns of parasitism.
4.4.1 Materials and Methods.
Except for host distribution, the observations were carried out
in exactly the same manner as that described previously. Similar
densities of parasitoids were used; that is, 1, 5, 10, 15 and 20
standardised females. - 160-
The total number of larvae used in Experiments 4.1 and 4.2 was
62. To provide an uniform distribution with each of the five patches
containing the same number of potential hosts, each swede disc was
inoculated with 12 second instar larvae, making a total of 60.
Reasonable comparisons could then be made between the two host distri-
bution patterns and their subsequent effect on levels of parasitism be
established.
4.4.2 Results and Discussion.
The most striking difference between the results of this experi-
ment and those described earlier in the Chapter (Sections 4.2.2 and
4.3.2) was that of the total number of hosts parasitised within the
eight-hour experimental period. The mean number of hosts parasitised
on the two distributions differed significantly (Figure 4.13: t-test, p < 0.05), more hosts being parasitised when they were aggregated.
This difference was only just significant at the highest parasitoid
density, 20. It has been established that aggregation, in general,
leads to higher search rates than random, non-directed search. At
high parasitoid densities the profitability of continual aggregation
in a clumped environment falls and a more even search strategy becomes
as, if not more, preferable.
Returning to the present experiment (Experiment 4.3), except for
a few cases when only one parasitoid individual was being observed,
there was no significant difference (ANOW, F-test, p > 0.05) between
the time spent on each of the five patches over either hourly intervals
or the whole observation period. In the case of one parasitoid,
significance is likely to have arisen as a result of the scarcity of
data rather than from any actual behavioural preference for any specific
host areas. For any single observation period certain patches were 24- ••n••
20- =OM 1
=Ow
4
0 1 5 10 15 20 Parasitoid density.
Figure 4.13 Differences in the total number of hosts parasitised
by various densities of parasitoids under conditions
of aggregated (al) and even (0) distributions. All
pairs of values are statistically significant (t-test,
p < 0.05). - 162 -
exploited more than others. However, no significant difference
(ANOVA, F-test, p > 0.05) was found among the mean number of hosts
parasitised per patch when the five replicates at each parasitoid
density were pooled. Host patch differences were consequently ignored
in all subsequent analyses. The lack of any significant difference between patches was, in itself, reassuring as it illustrated that the parasitoids were not showing an innate preference for any specific
region of the arena and that the aggregative response observed in previous experiments was a consequence of the hosts' distribution pattern.
The proportion of each hour spent on the patches is given in
Figure 4.14. It was only at the two highest parasitoid densities that there was a significant difference in time spent per hour over the eight-hour period (ANOVA, F-test,p < 0.05). At these densities the foraging wasps spent more time on the patches as the experiment progressed. On the aggregated distribution (Experiment 4.2) there was some indication that, during the later periods of the observations, the wasps were moving away from the more exploited patches at high parasitoid densities. No such pattern was observed on the even distri- bution. Consecutive visits were difficult to study in this set of observations as the single female wasp seldom made more than two visits to the same patch. Instead, different patches were visited and explored. From the limited data available the second visit was shorter (t-test, p < 0.001) than the first:
DURATION OF
First visit to a patch 53.0 ± 31.0 min (n=16)
Second visit to the same patch 18.9 ± 18.7 min (n=6).
Whether this was the result of some marking behaviour by the parasitoid was not established. 1•0-,
0 -9-
0.8-
0.2
0•1
0•0 8 7 Hours 6 5 from start 4 of observation. 20 15 10
Parasitoid density.
Figure 4.14 The allocation of searching time (mean ± 95 per cent
confidence intervals) on patches of equal host densities
over an 8 hour observation period at various parasitoid
densities. (Note that in order to display the relation-
ships more clearly both the 'parasitoid density' and
'hour' axes are reversed compared with Figures 4.5 and
4.12.) -1-5 -
- 2-0 -
-to
- 3-0 0 1 2 109 10 parasitoid density.
Figure 4.15 Relationships between the search rate, a', and the
density of searching Trybliographa rapae in a homogeneous
environment. Individual results are not given for clarity
(see text for details). - 165-
Searching efficiency was explored and analysed as was discussed in some detail in Experiment 4.2 (Figure 4.15). The all-inclusive interference relationship based on Equation 4.1 when T = 8 hours gave a mutual interference constant, m, of 0.37. This was not significantly different from that obtained in the heterogenous environment (m = 0.39) (t-test of regression coefficient, t = 0.01, p > 0.1). Again, even when behavioural interference had been abstrac- ted (Lines B and C, m = 0.30 and 0.29 respectively) the majority of the total interference phenomenon (78 per cent) still remained un- accounted for.
By considering each patch individually, using Equation 4.7, a virtually horizontal line (m = 0.03) was obtained between searching
efficiency and parasitoid density (Line D, Figure 4.15). This was
encouraging as it showed that the remaining interference had been
explained. The presence of such pseudo-interference, arising as a
result of the wasp's aggregative behaviour, was unexpected. The
apparent presence of pseudo-interference can be explained by the
observation that although no preference was shown overall for any
particular patch, each observational run produced certain host areas
which were exploited more than others. With each patch being con-
sidered separately such inter-patch differences were of considerable
importance. It was also puzzling that all the causes of interference
were identified in the present experiment while 61 per cent still
remained unexplained on the aggregated environment. The absence of
any intra-patch interference in the homogenous environment is not
easily explained unless such interactions only occur at the higher
host densities.
When estimates of searching efficiency, measured using Equation
4.7, were calculated (Table 4.5) and compared with those obtained Number of Search rate, a' Parasitoids Even Aggregated
1 0.021 ± 0.009 0.021 ± 0.005
5 0.030 ± 0.015 0.020 ± 0.009
10 0.020 ± 0.007 0.015 ± 0.007
15 0.025 ± 0.009 0.011 ± 0.003 *
20 0.023 ± 0.009 0.010 ± 0.003 *
Table 4.5 Comparison of the instantaneous search rate per
unit searching time, a', as measured by Equation
4.7, under conditions of even and aggregated host
distributions. Values given as means ± 95 per cent
confidence intervals of 5 replicates. * denotes a
pair of results differing significantly (t-test, p < 0.05). Time spent on patches Number of Parasitoids Even Aggregated
1 0.55 ± 0.13 0.59 ± 0.07
5 0.40 ± 0.19 0.66 ± 0.10 *
10 0.29 ± 0.06 0.60 ± 0.22 *
15 0.45 ± 0.17 0.55 ± 0.05
20 0.42 ± 0.05 0.55 ± 0.13
Table 4.6 Comparison of the proportion of total time spent
foraging on patches under conditions of even and
aggregated host distributions. Values given as
means ± 95 per cent confidence intervals of 5
replicates. * denotes a pair of results differing
significantly (t-test, p < 0.05). - 168- when hosts were distributed in an aggregated manner, the even distri- bution gave significantly higher values (t-test, p < 0.05) at the two highest parasitoid densities. This lends further support to the argu- ment that, as a result of over-aggregation and over-exploitation, parasitoids which distribute themselves evenly in the arena at high parasitoid densities are more efficient in finding hosts than those which show a marked tendency to aggregate as a consequence of host distribution.
There were no such significant differences between estimates of searching efficiencies at the lower parasitoid densities (Table 4.5).
With the higher number of hosts parasitised on the aggregated distri- bution than on the evenly distributed host-environment, a higher level of efficiency might have been expected on the former. However, as
Table 4.6 illustrates, at densities of 5 and 10 the parasitoids spent significantly more time on the patches when hosts were aggregated than when distributed equally. (The results for one female parasitoid did not show such significant differences, one of the five wasps used having remained on the host area for a considerably longer period of
time than any of the others, influencing unduly the mean value.) The
increases in both the levels of parasitism and the time spent on the patches therefore cancelled one another.
No consideration was given in Figure 4.13 to superparasitism and,
consequently, the total number of eggs laid at various parasitoid densities and host distributions. When levels of superparasitism at
the two distributions were compared, a significantly higher level was
found to have occurred at the two highest parasitoid densities when hosts were aggregated (Table 4.7). There were no such differences between levels of superparasitism at various parasitoid densities on
the even distribution (ANOVA, F-test, p > 0.05). It was concluded Parasitoid Number of eggs per host density Aggregated Even
1 1.00 ± 0.00 1.00 ± 0.00
5 1.04 ± 0.05 1.03 ± 0.06
10 1.14 ± 0.09 1.11 ± 0.10
15 1.38 ± 0.12 1.07 ± 0.07 ***
20 1.48 ± 0.14 1.06 ± 0.05 ***
Table 4.7 Comparison of the number of eggs laid per parasitised
host (mean ± 95 per cent confidence intervals) on both
aggregated and even host distributions. At parasitoid
densities of 15 and 20 there is a significant difference
in the two values (t-test, *** indicates p < 0.001). —15-
-20-
n•••••
5
- 30 I I 0 1 2 Log io parasitoid density.
Figure 4.16 The relationship between search rate, a ' , and parasitoid
density when levels of superparasitism are considered
(Line E). Data are from the aggregated host distribution,
Lines A and D as in Figure 4.10. - 171 - that while superparasitism played a negligible role in the inter- action when hosts were distributed evenly, it was of considerable importance at the higher parasitoid densities when hosts were aggregated.
At this point it is worthwhile returning to the interference levels explored in Experiment 4.2. Part of the 61 per cent of the total interference remaining unexplained may have arisen from the presence of higher levels of superparasitism. When the number of eggs laid, N rather than the number of hosts parasitised was egg•, considered, searching efficiency being given by
N. 1 1 a' =- E [ 1 ) 4.8 P T loge kN N i=1 t si i- eggi a further 38 per cent of the phenomenon was accounted for (Figure
4.16). The mutual interference constant, m, still had, however, a value of 0.09 and this, as considered previously, may have arisen from a combination of numerous, unquantified factors. It must be stressed, however, that the likelihood of such aggregation of parasitoids under natural conditions is highly unlikely and it is doubtful whether superparasitism is of as major importance as in the present context.
4.5. General Discussion.
Whether it be due to the active behaviour of the organism or to some heterogeneity of the environment, it is well known that the majority of organisms show some degree of aggregation. The potential importance of this spatial heterogeneity in the population dynamics of prey-predator and host-parasitoid interactions has been repeatedly established (Hassell, 1978 and reference therein). - 172 -
While foraging for its hosts, T.rapae showed a marked aggregative response, spending a higher proportion of time in areas where potential hosts were plentiful. Aggregative responses of this kind may arise as a result of a number of behavioural interactions. Some of these have already been considered in Chapter 2 (for example, Doutt,1959; Vinson,
1984a.; 1984b.). Hassell (1978) found it convenient for purposes of classification to divide host-finding into two distinct phases: the location of the host patches, followed by the parasitoid's searching response once within a host patch. The first category involves the perception by parasitoids of the existence of heterogeneity in the distribution of the host at a distance. Such location of host patches will usually depend upon visual or olfactory cues which may or may not be related to the density of host within the patch. Rotheray (1979) found that the parasitoid Callasipidia defonscolombei (Dahlbom.)
(Hymenoptera:Cynipoidea) was attracted to various concentrations of
its syrphid host by the odours produced by the syrphid's aphid prey while
Arthur (1966) illustrated how the ichneumonid Itoplectis conquisitor
(Say.) was attracted more to the red shoots of the Scots Pine, Pinus sylvestris (L.) (Coniferae:Pinaceae), than to the green ones. Further observations showed that the reddening of the shoots was in fact due to infestation by the parasitoid's host, the European Pine Shoot
Moth, Rhyacionia buoliana (Schiff.) (Lepidoptera:Eucosmidae
(Olethreutidae)).
The second category of behaviour underlying the aggregative response, that of the parasitoid's response within host patches, can be divided into three distinct types (Begon and Mortimer, 1981).
The first is illustrated by Clarke (1963) where female predators
(Syrphus spp. (Diptera:Syrphidae)) of one generation lay their eggs
in areas where there are high densities of prey, the psyllid
Cardaspina albitextura (Taylor) (Homoptera:Psyllidae). - 173-
Such behaviour ensures that the relatively immobile offspring are concentrated in the more profitable patches.
The second behavioural pattern involves an active change in the parasitoid's searching pattern in response to encounters with host items. This has already been discussed in some detail in Chapter 2.
Suffice it to state that there is often an increased rate of turning following an encounter with a host leading to the parasitoid remaining in the vicinity of the last host individual attacked (see Waage (1978) and previous discussion in Chapter 2). Because of the higher encounter
and turning rate on patches where resources are plentiful, parasitoids
(and predators) remain in these areas while they abandon low density
patches where the turning rate is low.
Finally, there is the tendency to abandon sites at which the
parasitoid's capture rate is low and to remain at sites where it is
high. Turnbull (1964), for example, found that the web-spinning
spider, Archaearanea tepidariorum (Koch.) (kraneae:Theridiidae), while
preying on fruit flies, D.melanogaster, within a large experimental
arena, modified their leaving rate in response to prey encounters.
This behaviour resulted in the predators congregating in patches of
high prey density.
The duration of a patch visit has attracted considerable interest
and various hypothetical models have already been mentioned in Section
4.1. Waage (1977) produced a detailed study of patch-time allocation
in the ichneumonid V.canescens and concluded that two factors played
a role in determining whether a wasp left a patch. The level of patch
odour determines the responsiveness of the wasp. This decays with
time spent on a patch, but is increased by an oviposition. The para-
sitoid leaves the patch when its responsiveness to that specific area
decays below a threshold level. - 174 -
As well as spending a shorter period of its total time on the low host density patches than on more densely populated areas, T.rapae also showed a smooth curvilinear transition in patch-time allocation from low to high host densities. Waage (1979) predicted this for
V.caneseens in his simulation model of the foraging behaviour of the ichneumonid. While in threshold rate models such as those developed by Hassell and May (1974) the change in the length of the stay on a patch is markedly discontinuous, Waage's model, which is primarily concerned with the effect of a contact chemical on the responsiveness of a parasitoid, predicts a smooth transition as the chemical stimulus from the patch increases with density even among those densities that are so low that the patch is abandoned prior to oviposition.
As a consequence of the increased searching times spent on the high host density patches an increased proportion of that area is searched, resulting in a higher proportion of hosts being attacked.
Hosts at lower densities have, as a consequence, a smaller probability of being attacked and can be assumed to exist in partial refuges. Such a phenomenon leads to a directly density dependent pattern of parasitism which provides a potentially powerful stabilising mechanism for host- parasitoid interactions (Hassell and May, 1973).
Recent work (Hassell, 1984) has shown that inverse density dependent relationships can also strongly promote stability. Hassell states that stability depends upon the extent on which the host popula- tion is unevenly exploited and thus arises from a partial refuge effect in which some hosts are more at risk than others. Such differential exploitation of the hosts may arise in several ways but all have the same effect of generating clumped rather than random distributions of hosts being attacked. - 175-
The strength of the directly density dependent pattern of para-
sitism by T.rapae of D.radicum was reduced as the number of parasitoids
foraging in the arena was increased. Areas which were refuges at low
parasitoid densities were exploited as more wasps were included in
the arena. The proportion of hosts protected is critical. If it is
too small, the refuge effect described above is negligible, parasitoid
foraging becoming essentially random. If it is too large, the level of
parasitism is not sufficient. Hassell (1978) has shown that refuges
where a constant number of the host population, rather than a fixed
proportion, is protected are more stabilising since at low densities
the proportion of the total population protected will be greater.
When the number of wasps in the arena was increased, interference
occurred. Subsequent analysis revealed that only a small proportion of
the total interference phenomenon was the result of actual behavioural
or mutual interference. Considerably more was found to be the result
of pseudo-interference arising from the differential exploitation of
the host patches. Hassell (1978) has argued that the dynamic balance between the processes of aggregation and interference should result in
an optimal parasitoid distribution at any given time. Such a concept was considered by Fretwell and Lucas (1970) and developed into the
'ideal free distribution'. By assuming that the distribution of para-
sitoids over a spatially heterogenous area is the outcome of two
opposing responses, those of aggregation in areas of high host densi-
ties and avoidance of interference by movement away from areas of high
parasitoid densities, they argued that it was possible to predict the
distribution of parasitoids. The name 'ideal free distribution' was
coined as the organisms are assumed both to be ideal in their judgement
of the profitability of each of the sites and to be free to move between
sites. According to this distribution pattern, parasitoids should dis-
tribute themselves so that each obtains the same food intake. - 176 -
A further consequence of increasing the number of foragers was to significantly increase the level of superparasitism, particularly on the high host density areas. This supported observations made in
Chapter 3 where conspecifics were found far more likely to super- parasitise than single females. When under pressure to find suitable hosts, females may oviposit regardless of whether the larvae have been parasitised previously. This has a detrimental effect on the efficency of the searching parasitoid but its importance in the field is doubt- ful as parasitoids seldom find themselves at such high densities.
There has been an increased tendency to incorporate the realistic assumption of non-random distribution of parasitism within the framework of mathematical models of host-parasitoid population dynamics (see
Hassell (1978) for examples). Little attention has, in the meantime, been directed to the levels and patterns of parasitism within an area where hosts are not aggregated but distributed equally among the available patches. Although the number of hosts superparasitised was significantly less when they (the hosts) were distributed equally, more hosts were parasitised, except at the highest parasitoid density where equal numbers of hosts were parasitised on both distributions, on the aggregated arena. Hassell (1978) has argued that the more prudent para-
sitoid (or predator) strategy is one where aggregation gives way to random search at high parasitoid densities, thus overcoming the over- exploitation of high density host areas as a result of the parasitoid's aggregative response. The development of population dynamic models on the basis of such experiments as those described have been criticised by a number of workers. Dempster (1975) has argued strongly that a real under- standing of factors determining the abundance of animals can be obtained only by the intensive study of populations in the field.
Chapter 5 sets out to consider this problem by exploring the T.rapae -
D.radicum interaction under field conditions to enable comparisons to be made between laboratory and field studies and to determine the relevance of the former to natural host-parasitoid interactions. - 178-
CHAPTER 5
PATTERNS OF PARASITISM BY Trybliographa rapae
UNDER FIELD CONDITIONS
5.1 Introduction.
In his introduction to 'The Dynamics of Arthropod Predator-Prey
Systems', Hassell (1978) comments on the difficulty of catergorising both host-parasitoid (or predator-prey) and competitive interactions under field conditions. While realising the dangers of over-
simplification (for example, constant environment, closed systems,
removal of interacting species other than those being studied) within
the confines of a laboratory experiment, he explains how many of the vagaries of the field situation are eliminated. Consequently, the
outcome of an interaction may be more simply classified. Further, by making simple models of the components of the system, their effect
on the overall dynamics of the interacting populations may be revealed.
Hassell supports the use of ecological theory as a means of contribut-
ing to a general strategy for biological control programmes as it is a means of identifying the factors which are necessary for a reduced and
stable pest equilibrium. However, as he states (Hassell, 1982b.),
'without well-chosen and properly executed field and laboratory studies,
little flesh can be added to the underlying framework and the subject
(population dynamics) will not develop coherently as a basis for ecology as a whole.' In contrast, Dempster (1975), as mentioned in the previous Chapter, believes that only limited progress can be made in constructing realistic population models and argues against the building of 'elaborate theories' on the basis of such studies. - 179-
Diamond (1983) reviewed the use of laboratory, field and natural experiments for various studies. Laboratory experiments provide a means of ensuring that independent variables are completely controlled and, as the literature illustrates, this is the main approach used by workers making detailed studies of two-species interactions. The major criticism of such an approach is that simple laboratory models become totally unrealistic in the face of most ecosystems being composed of multi-species interactions and external physical factors.
Field experiments often involve the manipulation of one or more variables, for example, the density of host species or the numbers of predators in exclusion experiments. Again, certain problems arise such as the dependence on annual and seasonal variation, generation variation and lack of spatial scale (particularly true for vertebrate populations). Also, the manipulation of multi-species interactions may not only affect the experimental species directly as envisaged, but also indirectly from the affects of such manipulations on other species.
Studies of natural systems escape most of the drawbacks of field
experiments but at the cost of sacrificing all manipulative control of
variables. The major difficulty with such experiments is that the
experimenter does not create a known difference between two situations
and has, instead, to decide what difference between two existing
situations is the salient one. However, natural studies do reveal the
end results of ecological and evolutionary processes that operate over
large spatial scales and long temporal periods.
Diamond (1983) concluded by commenting that each of the methods
has virtues and weaknesses, and limitations of scope that vary with
the species studied and with the questions being asked. In the case
of population dynamics and its modelling, the identification and - 180- description of regulating factors is of major consequence and frequently can only be satisfactorily explored experimentally under the restrictions imposed by laboratory observations. However, con- clusions made from such studies and subsequently supported by other methods are made considerably more robust.
The importance of establishing the relevance of laboratory work to the natural situation is unquestionable. However, collecting such data is not always as straightforward as it may appear to be.
Hassell (1978), in an attempt to find whether interference was an important factor in natural predator-prey interactions or simply a laboratory artefact, compared the values of m, the mutual inter- ference constant, from 25 studies made in the laboratory and in the field. Although it was the field results that provided the highest values of m, Hassell found that in all but one case the apparent interference could be due solely to sampling errors. It was only the work of Broadhead and Cheke (1975) on Alaptus fusculus (Hal.), a mymarid parasitoid attacking Mesopsocus unipunctatus (Mull.) and
M.immunis (Steph.) (Psocoptera:Mesopsocidae) eggs, that showed an interference relationship that was statistically significant.
The major criticism of any conclusions drawn from studies such as those described in Chapter 4 is that they are carried out in relatively small arenas over a short period of time. Levels of density which would not be reached under natural conditions may result in high levels of interference being recorded in the laboratory and the confinement of foragers to an experimental arena may lead to higher levels of parasitism than those reached if dispersal had been possible. The swede discs used so far in the present study has meant that all hosts have been available for attack. Whole swede plants may provide the larvae with physical refuges. The presence of whole - 181 - plants rather than cut discs would also produce a far more complex, multi-dimensional environment in which the parasitoid wasps would have to forage for potential hosts.
This Chapter sets out to overcome this criticism. By carrying out a series of observations on both field and naturally occurring populations of host and parasitoid, an attempt has been made to compare laboratory and field studies, and to establish the relevance of laboratory observations to what is believed to happen under natural conditions. The various studies were developed in an attempt to approach progressively the naturally occurring field situation. All field experiments were made on an area of cultivated land (Silwood
Bottom) at Silwood Park, Ascot, Berkshire.
5.2. Experiment 5.1: To determine the effect of host heterogeneity
on the levels of parasitism by Trybliographa
rapae under field conditions.
5.2.1 Materials and Methods.
The arena used in this experiment (Figure 5.1) consisted of a metal frame, measuring 100 cm x 100 cm x 50 cm, covered with Terylene netting. Excess netting was provided around the base of the arena and covered with soil. An arm-hole was cut at the top of the arena to facilitate the introduction of the experimental, female parasitoids.
An area of crop-free soil was used for the experimental arena and cleared of any weeds immediately prior to the study. Five, 8-week old, nursery-grown swede plants (Napus brassica var. napobrassicae cv.
Acme (Tozer)) were transplanted into the arena in a similar pattern to that used in the laboratory and left for 48 hours to establish.
Subsequently, second instar larvae, standardised as described previously - 182-
lm •
Swede Swede Metal frame covered with 50 cm terylene netting.
i s
% /I t%.....) % , %...... ,
Figure 5.1 The experimental arena used in Experiment 5.1. - 183- and in similar numbers to those used in Chapter 4, were placed around the swede root and left for 24 hours to burrow into the host plant.
Throughout this period the plants were covered to prevent attack by native cabbage root flies and other pests.
Prior to the start of the experiment the soil surface around the swede base was examined for any dead larvae. These were removed and replaced by live individuals. Standardised female wasps were intro- duced in numbers ranging from 5 to 20 via the arm-hole and left to interact with the host population for 48 hours. At the end of this period the wasps were collected. The swede plants and the surrounding soil were removed and placed in individual plastic sandwich boxes.
In those cases where all the wasps were not collected at the end of the experimental period care was taken while examining the contents of the sandwich boxes to ensure that no wasp still remained to interact with the host population. After a further 24 hours the swedes were carefully dissected for larvae and the level of parasitism recorded.
Parasitoid densities of 5, 10, 15 and 20 per experimental arena were repeated 10, 8, 5 and 5 times respectively.
5.2.2 Results and Discussion.
Of the 28 arena experiments, dead larvae were recovered on only four occasions. In two cases the larvae were parasitised. As it was not possible to determine the actual 'time of death' this was not taken into account in subsequent analyses, all larvae being assumed equally likely to have been attacked. When percentage parasitism was plotted against both parasitoid and host densities (Figure 5.2) the general pattern of parasitism found in the field (a.) closely resembled that of the laboratory (b.). Two main differences were found to exist.
Firstly, except at a parasitoid density of 5, a significantly higher Figure 5. 2 a.) Levels of parasitism (in terms of percentage
parasitism) reached by adult parasitoids in the
field on patches of differing host densities,
parasitoid densities ranging from 5 to 20.
b.) As for (a.) but for laboratory observations
described in Chapter 4. 70 —
60 -
50 -
40 - MEM
30 -
20 - 1 10 -
32
Nt. 16
5 10 15 20
Pt.
60 - b.
50 -
40 -
30 -
20 -i K IN K k 10 -, 1\ \
32 Number hosts per patch, Nt. 16 1 Number of searching parasitoids,Pt. 40 —
0 5 10 15 20 *** ** ** ***
Parasitoid density.
Figure 5.3 Comparison of the total number of larvae parasitised
per arena under field 013) and laboratory (10)
conditions at various parasitoid densities ( mean ±
95 per cent confidence intervals are given, ***
indicates p < 0.001 (t-test); **, p < 0.01). Parasitoid Mean number of eggs per parasitised host density Field Laboratory
5 1.05 ± 0.04 1.04 ± 0.04
1 0 1.06 ± 0.03 1.14 ± 0.09 *
15 1.11 ± 0.05 1.38 ± 0.12 *
20 1.06 ± 0.04 1.48 ± 0.14 *
Table 5.1 A comparison of the levels of superparasitism
at various parasitoid densities under both
field and laboratory conditions. Mean ± 95
per cent confidence intervals are given;
* indicate data values significantly different
at p = 0.05 (see text for details). - 188-
level of overall parasitism was recorded in the field (Figure 5.3).
Over an equal experimental period of eight hours a higher level of parasitism would have been expected in the laboratory as the wasps would have required a longer period of time to locate potential hosts in the field. However, over a 48-hour period it was reasonable to find that, as the wasps were enclosed in the arena for a longer period of time, more hosts were located and parasitised.
In the comparable laboratory observations high parasitoid densities resulted in higher levels of superparasitism. When this phenomenon was explored in the field there was no significant difference in the mean number of eggs laid per parasitised host at the four parasitoid den- sities (MOM, F-test, p > 0.05). These results, along with their comparable values from Experiment 4.2, are given in Table 5.1. The difference in levels of superparasitism between the two environments may have been a contributing factor to the higher level of overall parasitism observed in the field.
The second major difference between field and laboratory results was that of the pattern of parasitism, particularly at the higher levels of parasitoid density. As Figure 5.2 illustrates, the low density host patches were exploited to a considerably higher degree in the field situation. The longer experimental period could have contributed substantially to this difference but, when taken into consideration with the absence of any significant level of super- parasitism by T.rapae, it suggests either the presence of a strong degree of dispersion from the high density host patches at high para- sitoid densities under field conditions, or a weaker aggregative response arising from a reduction in the chemical stimuli emanating per unit area from the swedes. - 189-
An estimate of the searching efficiency of the wasps was obtained from Equation 4.1. Since the wasps were not observed throughout the experimental period no estimate of the actual time spent foraging, or the allocation of patch time, was available. It was, therefore, taken to be 48 hours. The estimated searching efficiencies for various parasitoid densities under both laboratory and field conditions are given in Figure 5.4. The efficiency of the parasitoid in searching for potential hosts was significantly lower in the field than in the laboratory (t-test, p < 0.05) at all parasitoid densities. No con- sideration was given while estimating a' to the fact that the index of searching efficiency is area dependent. Since there was an approxi- mately four-fold difference in the areas of the two arenas (laboratory and field), a lowering of efficiency in the larger sized enclosure was not unexpected. Also, as swede plants presented the foraging para- sitoids with a more multi-dimensional substrate to forage on, the wasps were likely to encounter far more difficulty in locating hosts burrowing into a swede in the soil than they were in small, thin discs of swede placed on sand in the laboratory.
Another feature of interest was that changes in parasitoid density appeared to have a more marked effect on searching efficiency in the
laboratory than in the field. When searching efficiency, a', was plotted on a logarithmic scale against parasitoid density, field
results gave a mutual interference constant value of 0.14 (Figure 5.5).
The comparable value obtained during the laboratory studies was 0.39.
As the differential exploitation of patches was also not as marked in
the field as in the laboratory, particularly at high parasitoid den-
sities, it would appear that the aggregative response observed in the
laboratory was not as strong under field conditions. However, as
Figure 5.2(a.) illustrates, there was still a definite directly density
dependent pattern of parasitism with high density host areas being 10-0—
. 8-0- — o I o o.- m
6-0 n C.) C .m Zi I 0 co 4-0- C ..2 C.) (1 m I co 2-01
0-0 n n n 5 10 15 20 Parasitoid density.
Figure 5.4 Estimates of searching efficiency, calculated using
Equation 4.1, at various parasitoid densities under
field (0) and laboratory (III) conditions. Mean
values ± 95 per cent confidence intervals are given. - 2-0 - • : • - 2-2- 2 0 •
•2 • • -2-4 - • . ' to
3.- U • m=0-39 C e3 .._C., - 2-6a • I) 7. • "iii
CD C :E • 0 - 2-8- ei • e 0 a 2 0 0 al o -, 0 4 03 0 -3-0- 0 4 0 0 0 2".'"•• 0 2 0 0*""+0 ...... m=0-14
0 02 - 3-2- 0
-3.4-. i 1 v i I I
0-0 0-3 0-6 0-9 1-2 1-5 Logio parasitoid density.
Figure 5.5 The interference relationship between the searching
efficiency ( log 10 a' ) and density of searching
parasitoids estimated from both field (0) and
laboratory (• ) observations. - 192- exploited to a higher degree than the low density ones. Such differential exploitation was less marked at the highest parasitoid densities where patches appeared to be exploited at more or less equal levels.
5.3 Experiment 5.2: To determine the levels of parasitism by
naturally occurring parasitoid populations
on manipulated host densities.
5.3.1 Materials and Methods.
The next step in the experimental progression towards the natural situation was to use the native parasitoid population on manipulated host numbers. During the summers of 1983 and 1984 (late June - early
September), nursery-grown swedes (8 - 10 weeks) were transplanted into a clear area between two swede crops and inoculated with second instar cabbage root fly larvae. They were then left in the field for 14 days to be parasitised by the native T.rapae population. At the end of the period the swedes and surrounding soil were collected and brought into the laboratory for examination of the cabbage root fly hosts.
5.3.2 Results and Discussion.
As protective arenas were not being used in this experiment it was necessary to establish to what degree inoculations by native, fecund cabbage root fly females would affect the experimental observa- tions. Swedes, free of cabbage root flies, were transplanted into the field and left for 14 days. At the end of this period they were brought into the laboratory and examined for any larval activity. This procedure was repeated at various intervals during the experimental period. In a few cases the soil surrounding the swedes contained eggs but in only two
(out of 40) samples had swedes been actually attacked by larvae. These were in their first instar and as such could easily be distinguished - 193- from the experimental second instar larvae. (The first instar larva has no anterior spiracles while second and third instars have both anterior and posterior spiracles. The posterior spiracles of the second instar differ from those of the third in having only two openings in each spiracle instead of three.) The presence of eggs and extra larvae may have increased both predator activity and para- sitoid foraging (the larvae producing a higher concentration of chemical attractant from the frass) but these effects should have been unbiased and equal on all host densities used in the experiment. Consequently, this was not taken into consideration.
When the experimental larvae were collected after 14 days some individuals were missing. As this problem had not been encountered when larvae were collected from the field cages (Experiment 5.1) it was not thought to have arisen from actual experimental procedure or the experimenter's inability to find the larvae. For both years, when the proportion of larvae lost was plotted against the initial larval density a significant relationship was obtained (Figure 5.6). Food limitation or inter-larval competition for resources were not considered to be causal factors for such a relationship, laboratory cultures having shown that a single swede can support severe larval infestations.
Although a proportion of the larvae may have starved as a result of their unsuccessful attempts at entering the plant tissues it is un- likely that this would show any marked density dependence. Schoene
(1916), Gibson and Treherne (1916) and Smith (1927a.) have all reported that mortality in the larval stage can be caused by predatory ants, beetles and other anthomyiid larvae and the observed relationship may have been the result of the aggregative response shown by one or all of these larval predators. The enclosed environment of Experiment 5.1 would have reduced such predator activity to a minimal level. This mortality factor will be considered in further detail in the following
Chapter.
Figure 5.6 The relationship between larval disappearance and
initial larval density in Experiment 5.2 during
the summers of a.) 1983 and b.) 1984. - 195 -
a.
0 •8 - 1983. 0.7-
0-6-
/2/ 0 -5- • •2• 04-a •
0.3 -
0 .2-
0.1- •3 0 0'0 ..1' .9/..3 llirli 0 10 20 30 40 50 60 70 80
b.
0 -8- 1984. 0.7.4 . • z 0-6- • 1 • • 0 -5- • • • 02 • 02 0-4- •2 •2 • • 0.3- • 03 02 • 0 .2- • •2 0. 1 -
0 • 0 "Ill 1111 I 1 0 10 20 30 40 50 60 70 80 Initial larval density. - 196 -
When the proportion of larvae parasitised by T.rapae in the summer of 1983 was plotted against the initial larval densities there was no significant relationship CE - 2.27, p > 0.05). There was a direct relationship between proportion parasitised and initial host number in 1984 (Figure 5.7). Whether this was the most accurate means of considering the results is uncertain. If larval disappearance was the result of a combination of predation and inability to establish in the swede plant, both occurring in the soil surrounding the swede, then it is justifiable to consider the level of parasitism as a propor-
tion of those larvae collected at the end of the experimental period.
Thus it was assumed that predation was, to a large extent, restricted
to outside the swede tissue where T.rapae does not forage nor parasitise.
By making such an assumption, both years showed a markedly significant
density dependent response (Figure 5.8a. and b.). This further supports
the conclusion drawn from both laboratory (Chapter 4) and field experi-
ments (Experiment 5.1) that a higher level of parasitism occurs when
host densities are high.
Of the 1916 larvae dissected during this experiment (652 of which
were parasitised) only two contained more than one parasitoid egg. It
may be that some eggs had been cannibalised during the 14 day period,
their remains having disintegrated. Only one adult T.rapae emerges
per parasitised host and Eijsackers and Bakker (1971) showed for
another cynipid, Pseudeucoila bochei (Weld.), that physical attack may
be a means by which supernumerary larvae are destroyed. Wishart and
Monteith (1954) noted the presence of small but distinct and well-
sclerotised mandibles on the first instar larvae which would be
suitable for such attacks. With such a negligible level being
observed, superparasitism is, however, unlikely to be a common
occurrence in the field. • • • .2 • • •2
•2 •2 • 02 •
20 30 40 50 60 70 80
Initial larval density.
Figure 5.7 The relationship between the proportion of Delia
radicum larvae parasitised by Trybliographa rapae
and the initial number of larvae open to attack.
Data from observations made during Summer 1984. Figure 5.8 The density dependent relationship between the
proportion of cabbage root fly larvae parasitised
by Tryblingrapha rapae and the number of larvae
collected after 14 days interaction. Results are
given for a.) 1983 and b.) 1984.
a. 1-0-, • 1983 0-9-
0-8-
0-7- • 0-6-
0-5-
0-4- • • V#0 • 0-3- % •• 02 • • • • 0-2- %et • 0 03 • 0-1-
5 2 410.0 1 0-0- 1 I I I 0 10 20 30 40 50
b. 0-8-, 1984 0-7•
0-6- • • • . •• • • 0-5- • • • •• • •2 • 0-4- • • • • • 0-3- •2 2 .2 • 0-2- •
e2 0-1'
25 2 0-0 •••• i 1 I I I 0 10 20 30 40 50 Number of larvae collected. - 200 -
5•4 Experiment 5.3: To determine the patterns of parasitism
within a naturally occurring population
of the cabbage root fly and its parasitoid
27rybliographa rapae.
5.4.1 Materials and Methods.
Sampling for levels of parasitism within a natural population during the growing season is difficult as one is dealing with a
temporal as well as a spatial scale. Generation overlap also
results in considerable confusion over which population levels
should actually be considered. In an attempt to avoid such problems
samples were taken from 1981 to 1984 of the overwintering cabbage root fly population at Silwood Park (1981 data from P.M.Reader, un- published). Pupae of the overwintering generation of the cabbage root fly can be sampled from October to March, during the obligatory winter diapause.
During the November of each year 20 - 40 swede plants, randomly chosen from various swede growing areas at Silwood Park, were sampled for overwintering pupae. As an attempt was to be made to determine whether or not the cabbage root fly populations were distributed in a non-random manner the number of samples taken from a swede patch in
1983 and 1984 (40) was larger than for the previous two years (22 and
20). By comparing the pupae's spatial pattern with that predicted by the negative binomial, a mathematical description of a clumped distri- bution, some indication of the degree of host aggregation could be obtained.
The soil around each swede was examined, the sampling unit being a square area measuring 25 cm by 25 cm with the swede plant at its centre. Although Hughes (1960) used a 15 cm diameter core taken from - 201 - under a harvested swede plant and believed it to give relatively accurate measurements, Finch, Skinner and Freeman (1978) found that
15 cm diameter samples, although adequate for most Brassica plants, resulted in the recovery of only 40 - 50 per cent of the pupae in
swede crops. Since they also found that 80 - 100 per cent of the pupae formed were present in a 5 cm collar of soil around the plant a 25 cm sample was considered sufficient. That this was so was shown by taking samples at 5 cm intervals away from the plant (Figure 5.9).
Ninety five per cent of the pupae were found in the 10 cms adjacent
to the host plant. The soil was sampled to a depth of 15 cms.
Observations made during the present study (Table 5.2) indicated that at Silwood no pupae were found deeper than 10 cm. Similar work at
N.V.R.S., Wellesbourne has shown that most of the overwintering pupae are formed at a depth of 5 - 7.5 cm (Finch and Skinner, 1980).
Pupae were separated from the soil by stirring each sample in a
large plastic container full of water. The water and floating material was then poured onto a 20 mesh/25 mm sieve on which any pupae present were rinsed, cleaned and collected. Empty puparia were ignored as being remnants of past generations. The pupae from each sample were
counted and placed in 80 ml plastic containers with damp vermiculite.
Coaker and Wright (1963) showed that field collected cabbage root fly pupae required 15 - 18 weeks at 5°C to complete their diapause develop- ment and Collier and Finch (1983) have shown that the pupae require a
further 14 days at 20°C for most of the flies to emerge. On emergence
the insects were removed from the container, sexed and recorded.
Past studies (e.g. Wishart,1957; Read,1962; Abu Yaman,1960;
Bromand,1980) have been unclear on whether levels of parasitism have
been expressed as a percentage of the live insects or as a percentage
of the total number of pupae. Finch and Collier (1984) comment on the
need to standardise estimates of the levels of parasitism within a 1•0
.-:. • mi ; 0 limmolnI
a.
••n•n• a) a 0.6- 0.=
.6 0.4- c .o t o o. n.2 0.2- IIMnImmr
n n 0.0 r-T-1 ii IT mi 0-5 6-10 11-15 16-20
Distance from swede plant (cm).
Figure 5.9 The distribution of pupae around a swede plant.
Data taken from 10 samples; mean ± 95 per cent
confidence intervals given. Depth below Proportion of pupae soil surface collected per swede sample (cm)
0.1 - 2.5 0.17 ± 0.12
2.6 - 5.0 0.44 ± 0.10
5.1 - 7.5 0.32 ± 0.08
7.6 - 10.0 0.07 ± 0.06
Table 5.2 The proportion of pupae collected per swede
sample at various depths below soil surface.
Results are given as mean ± 95 per cent
confidence intervals of 18 samples.
- 204 -
population and suggest the use of the percentage of the total pupal
number. To obtain absolute levels of parasitism, after 28 days at
20°C puparia from which no insects had emerged were dissected and the
contents noted. At this stage it was still possible to determine
whether a puparia contained the remains of a cabbage root fly pupa or
that of a natural enemy.
5.4.2 Results and Discussion.
It is now widely recognised that most animal species are not
randomly dispersed throughout their habitat, the negative binomial
and other contagious distributions having been successfully used to
describe their dispersion in space (Neyman,1939; Anscombe,1949; Bliss
and Fisher,1953; Bliss,1971). Of these, it is perhaps, the negative
binomial that is best known.
To fit a negative binomial distribution to sampling data requires
an estimate of k, a measure of the amount of clumping often referred
to as the dispersion parameter, in the expression
x— 4 (k + x - I)! x )x 5.1 19 (x) = 1 - ) x ! (k - I)! — k x +
where P is the probability of x individuals being found in a (x) sampling unit. A preliminary estimate of k may be derived from
the equation 2 k- 5.2 • S x
This estimate is then used as a starting point for substitution in the
maximum likelihood equation Ax n loge (1 + ) = E ( ) 5.3
where A is the sum of all frequencies of sampling units containing x
more than x individuals (e.g. A 6 = E ; 7 +i8 +....44n ) and n is the total
number of sampling units. The two sides of the equation must be made Figure 5.10 Frequency distributions of the number of cabbage
root fly pupae found per swede plant for November
1983 and 1984. Observed data and frequencies
predicted by the negative binomial (broken line)
are given. Estimated value for k (see text for
details) for 1983 and 1984 was 0.8 and 0.6
respectively. s 1983 e a- I ••n11, • I i -V, I
6 1
s In11,
*ek 4... 0.,
411n•n hir\' n
'OS
gmalmmor 2 - —S ... 4,, S. • -48,...,..-.-. • ..------{4._,. • H n • ....._.• • _
o 5 10 15 20 25
s
le s 1984 8 - I I I I I i i 6 - I
l e t % 4-. --.1 4 % . 1n11, e%
... • •n••nn 2 - ..11". •• -. 5, -o. -S -5. -O.. e _ •fl• _ .4. ••••-0- o o 5 10 15 20 25
Number of pupae. - 207 -
to balance by iteration and, when determined, provides a value of k
that may be considered to be of reasonable accuracy (Southwood,1978).
The frequency distributions for 1983 and 1984 are given in
Figure 5.10, the broken line indicating the expected distribution obtained by substituting the estimated value of k (from Equation 5.3)
into Equation 5.1 above (Jeffers(1978) provides a detailed example of
such a calculation). For 1983 and 1984 the estimated values of k were
0.8 and 0.6 respectively.
Having calculated the expected frequencies, these may be compared
2 with the actual values using a x -test (Bliss and Fisher,1953; Elliott,
1977). For both years no significant difference was shown between
2 observed and calculated results (x -test, p > 0.05). Southwood (1978) argues that such a comparison between actual and expected frequencies may be distorted by irregularities due to chance, particularly so in
the frequencies of the higher counts (x > 3). Southwood suggests the use of two alternative tests based on the difference between the expected and actual moments (mean, variance or skewness) compared with
their standard errors (Anscombe,1950; Bliss and Fisher,1953). Follow- ing Evans (1953), when considering data with small means, unless k is large, the most useful and efficient test is that based on variance
(U-test), while for other values of and k the test based on skewness
(T-test) should be used. His paper (0.206) contains a chart which, by plotting the values of ./1( in a study against X', indicates which method
is preferrable.
In the present study the test based on the second moment was the most appropriate for both years. This involved calculating the statis-
tic U which is the difference between the actual variance and the
expected variance and is given by 2 2 — U = s - ( x - ) 5.4 where k is the estimated value of the parameter. For perfect agreement with the negative binomial, U and T have expected values of zero.
Agreement is accepted, however, if the values of U and T differ from
zero by less than their standard error. For both cases U (1983 -13.25;
1984-22.90) was significantly less than its standard error (1983 -
15.81; 1984 - 34.76) and the negative binomial was accepted as a
satisfactory model, supporting earlier conclusions.
Increases in the value of k above 1 indicate that the distribution
is approaching, and eventually, as k approaches infinity, becomes
identical with, that of the Poisson. Fractional values of k indicate a distribution tending towards the logarithmic series which occurs when k is zero. Various workers (Morris,1954; Waters and Henson,1959;
Harcourt,1961) have found that the value of k is often influenced by the size of the sampling unit and stress that for any comparisons the same sized unit must be used. Also, the value of k varies with habitat and with development stage. Harcourt (1961) found that for the small cabbage white butterfly, Artogeia (Pier-is) rapae (L.) (Lepidoptera:
Pieridae), k varies with both the development stage and mean density within a range of 2.3 to 7.8. Previous studies on the spatial pattern of the immature stages of the cabbage root fly have indicated a clumped population. Mukerji and Harcourt (1970), for example, found the nega- tive binomial to provide the best description of pupal distributions, the values of k changing slightly with development stage as follows: egg, 0.78, larva, 0.71 and pupa, 0.84. Such aggregation could be due to a behavioural cause such as the female cabbage root flies tending to lay eggs in one locality or to the heterogeneity of the environment
- only certain plants being suitable for oviposition.
Having established the clumping tendency of cabbage root fly pupal populations, the pattern of parasitism was explored by plotting the proportion of pupae parasitised against the number of pupae Figure 5.11 The relationship between parasitism of Delia radicum
pupae by Trybliographa rapae and the host population
per plant as obtained from swede crops sampled at
Silwood Park during 1981 - 1984.
a.) 1981 Equation of line: y =0.03x - 0.04
b.) 1982(A) Equation of line: y =0.02x + 0.05
c.) 1982(B) Equation of line: y =0.03x + 0.10
d.) 1983 Equation of line: y =0.02x - 0.02
e.) 1984 Equation of line: y =0.02x + 0.03. - 210 -
a. b. 1•0- 1 .0-
0.8- 0.8-
0.6- 0.6- • • 0.4 - • • 0-4- • • • 0 2- .3 0.2- . 02 , • .2 ' 4 2, ••••• n 00 I I 1 0 .0 -• ••je T I n
0 10 20 30 0 10 20 30
C. d. 1 . 0 -• 1 . 0 -'
0.8- 0.8- • 0-6- 0•6 7
• ...././... • 6 • 2 0.4- 0.4- • • • 200./ 0.2- / 0.2- 32 0.0 •• i v i 0 .0 •••71n1:47:.9..•...•1 I 1 0 10 20 30 0 10 20 30
e. 1.0-
0.8-
0.6- •• • • 0-4-. 2 2 • • e e2 0.2- • • 943 0•0 ..ir•••• n • I I 1 0 10 20 30
Number of pupae. -211 -
collected per sampling unit. All five samples yielded significant
density dependent responses (Figure 5.11: F-test for significance
from b = 0, p < 0.05), the parasitoid causing a higher level of
mortality in patches where hosts were relatively abundant. Although
linear over the data range, it is important to note that the relation-
ship between proportion parasitised and host density is likely to rise
non-linearly to an upper asymptote. The relationship should, therefore,
not be extrapolated beyond the bounds of these data.
Hassell (1980), while exploring the interaction between the winter
moth, Operophtera brumata (L.) (Lepidoptera:Geometridae), and its
parasitoid Cyzenis albicans (Fall.) ()iptera:Tachinidae), found that
the slopes of the density dependent relationships were inversely
correlated with the mean density per year. He found a greater relative
difference in the levels of parasitism between trees in years when winter
moth was scarce than in those when they occurred in large numbers. It
appeared that C.albicans discriminated more markedly between trees of
different host densities when the winter moth was scarce but searched
more evenly between trees when the host insect was abundant. Such a
pattern was not observed with T.rapae, the level of density dependence
remaining relatively constant (F-test, p > 0.05) over the four years.
This may be attributed to the mean pupal density per plant showing
little variation over the time period in question (Table 5.3).
As well as numbers of T.rapae, data were collected on other parasitoids of the cabbage root fly. During November 1982, in Plot B,
5 per cent of the pupae were parasitised by a pupal parasitoid, the
ichneumonid Phygadeuon trichops (Thomson). Aleochara bilineata was recorded in each of the four years in levels ranging from 5 to 20 per cent. Subsequent analysis of these data (P.M.Reader, unpublished data) yielded density independent and inverse density dependent responses. - Year x
1981 5.36 ± 1.52 0.029
1982A 7.15 ± 2.51 0.017
1982B 8.75 ± 3.92 0.025
1983 5.55 ± 2.34 0.021
1984 7.20 ± 2.72 0.023
Table 5.3 The mean number of pupae (± 95 per cent confidence
intervals) collected per swede plant during 1981-1984.
The degree of density dependence, as determined
by b, the gradient of the linear relationships
in Figure 5.11, are also given. - 213 -
Patterns of parasitism by this parasitoid are considered in greater detail in the next Chapter.
5. 5 General Discussion.
The scarcity of comparable field and laboratory studies in the literature has made it difficult to establish, to any degree of certainty, whether laboratory investigations carried out on the components of host-parasitoid and prey-predator population dynamics have any relevance to what is observed in the field. There are a number of well-explored field population studies (e.g. the knapweed gall-fly, Vrophora jaceana (Hering.) (p iptera:Trypetidae) (Varley,
1947,1971; Varley and Gradwel1,1968), the winter moth (Hasse11,1980) and the cinnabar moth, 1Vria jacobaeae (L.) (Lepidoptera:Arctiidae)
(Dempster,1971)) and laboratory studies (see Hassell (1978) for examples) are plentiful. However, few attempts have been made to relate these two sets of data. Using the cabbage root fly -
Trybliographa rapae interaction, an attempt has been made in this
Chapter to explore the system under field conditions and compare results with those obtained in the laboratory (Chapter 4).
It was obvious from laboratory, field and natural population studies that T.rapae exhibited a density dependent response where a higher proportion of cabbage root fly larvae were parasitised in those areas where they were most dense. This is in contrast with the findings of Morrison and Strong (1980) who inferred from studying field patterns of parasitism that most parasitoids do not generate density dependent patterns of parasitism. The density dependence exhibited by T.rapae has been shown from laboratory observations to be the consequence of the marked aggregative response shown by the parasitoid, resulting in it spending a disproportionate length of its foraging time on patches of high host density. The response weakened - 214 -
as parasitoid density was increased, the distribution of attacks
becoming more equally divided among the patches. This increased
tendency to disperse and distribute themselves in a more random
manner, particularly at high densities, was strongest among para-
sitoids under experimental field conditions.
It is worth noting that a marked aggregative response on its own
does not indicate the presence of directly density dependent para-
sitism. Hassell (1982c.) showed that aggregation of total foraging
time may generate patterns of parasitism ranging from direct to
inverse density dependence, as the proportionate contribution of
handling time to total time increases. Waage (1983), in a detailed
field study of the foraging time allocation by a population of two
species of ichneumonid wasps (Diadegma eucerophaga (Horstmann) and
D.fenestratis (Holmgren)) on plants containing different densities
of their hosts, caterpillars of nutella xylostella (L.), found that
the parasitoids were spending more time on higher density patches,
thus exhibiting a clear aggregative response. Despite such aggre-
gation the wasps showed no tendency to exploit the most profitable
patches to yield density dependent patterns of parasitism. Waage
suggests two mechanisms to explain this observation. Firstly, that wasps may be attacking the same proportion of hosts per unit time at
all densities, distributing their eggs in a manner that does not lead
to an increase in per cent parasitism. This could arise from there being relatively more superparasitism at high host densities. Secondly, wasps may be attacking a lower proportion of hosts per unit time at higher densities as an increasing fraction of that time is spent in
activities other than search. He concludes that the strong aggre-
gative response of field populations of Diadegma spp. may be largely
attributable to handling time and related behaviour, with actual
searching time varying little between densities, leading to density
independent patterns of parasitism. - 215 -
Estimating the parasitoid's searching efficiency in the field proved difficult. The only proper means of assessing natural patterns of time allocation and its consequences is by direct field observation of foraging parasitoids (see Waage,1983). Such a detailed observational study was not possible in the system being studied, both the inter- action time was too long and the foraging habits of the parasitoid made it difficult to observe. Consequently, the most approximate estimate of field efficiency was that obtained from the field arenas. Not surpris- ingly perhaps, searching efficiency in the field was far lower than in the laboratory. The larger sized arena, the presence of whole swede plants and climatic factors presented the foraging parasitoid with a far more complex multi-dimensional environment than that encountered
in the laboratory. The exploitation of plants inoculated with various host numbers, particularly at high parasitoid densities, appeared to be less marked in the field than in the laboratory. It may be that a swede plant inoculated by, for example, 32 second instar cabbage root fly larvae did not release as much attractant or arrestment chemical per unit area as the same number of larvae in a small swede disc, resulting in a somewhat weaker aggregative response.
Levels of superparasitism were higher in the laboratory, contri- buting substantially to the lowering of parasitoid searching efficiency at high host density. A far lower level of interference, as described by m, the mutual interference constant, occurred under field conditions and was assumed to arise from a combination of both behavioural and pseudo-interference.
It is obvious from these results that there was considerable
qualitative agreement between laboratory and field observations of the Delia radicum - TY0liographa rapae interaction. Although - 216- quantitatively the degree of differential exploitation of infested areas and resulting interference among individual foragers may differ and not be as pronounced in the field as in the laboratory, the general density dependent pattern of parasitism is unquestionably present under both conditions. The contribution of this density dependent response to population regulation is considered further in the next Chapter when it will be assessed in relation to other mortality factors. - Z17-
CHAPTER 6
MORTALITIES AFFECTING CABBAGE ROOT FLY POPULATIONS
6.1 Introduction.
It is widely assumed that natural enemies are important in the
regulation of insect populations (for example, Huffaker,1970; Varley
and Gradwel1,1970; Southwood and Comins,1976; Hasse11,1978; Strong,
Lawton and Southwood,1984) and the detection of regulatory processes
acting on natural populations has long been a major concern in popula-
tion ecology. Recently, Dempster (1983) has challenged the view that
natural enemies are important as regulatory factors; in particular,
in the regulation of temperate Lepidoptera populations. By examining
a number of Lepidopteran population life-tables Dempster found that
only three studies revealed natural enemies as density dependent
factors. Hassell (1985) believes that life-table studies such as
those used by Dempster, based only on average population densities per
generation, are an unreliable means of identifying density dependence
acting primarily by creating differential susceptibility to parasitism
within generations. He argues that, ideally, life-table studies should
aim, not only to cover as many generations as practicable, but should
also take account of spatial and other forms of within-generation
heterogeneity.
A number of life-table studies for the cabbage root fly already
exist (Hughes and Salter,1959; Hughes and Mitche11,1960; Mukerji,1971
and Benson,1973) but all are based on average populations per genera-
tion. Any density dependent mortality on a spatial scale within generations (for example from plant to plant) may well have gone undetected. Although spatial heterogeneity is now recognised as an important contributor to population regulation, the majority of field - 218 - studies still overlook this in their design. It is clear that the detection of within-generation processes of this kind requires life- table data stratified both in space and time. Without these there is the very real risk that the true causes of popaiation regulation will go undetected.
Having explored the effects of parasitism by T.rapae under both laboratory (Chapters 3 and 4) and field conditions (Chapter 5) this
Chapter is concerned with the examination of the relative contribution to the population dynamics of the cabbage root fly of various mortality factors operating spatially from plant to plant within a generation.
The major causes of mortality affecting cabbage root fly populations
examined are (1.) egg predation by carabid and staphylinid beetles,
(2.) larval predation, parasitism and failure of larvae to find a
suitable host plant and (3.) pupal predation, parasitism and failure
to eclose.
Solomon (1957) stated that it is density dependent processes such
as those considered in the previous two Chapters that account for the
regulation of populations. Such processes may function over all or
most of the density range of subject populations or be restricted to
only a part of the range. The effects of some density-related processes
increase with population size; the effects of others diminish. Most
of the attention paid to density-related processes has been concentrated
on those with subtractive effects that intensify as population numbers
increase. It has been conclusively shown that such processes are
capable of providing stabilising mechanisms that effectively oppose
the indefinite increase of population numbers. As mentioned in Chapter
4, Hassell (1984) has shown that inversely density dependent patterns
of parasitism per patch can also strongly promote stability in host-
parasitoid interactions. He comments that the stabilisation of an - 219 - interaction is dependent upon the degree to which the host population is unevenly exploited. This differential exploitation of the host population may arise as a result of parasitoid behaviour (for examples see Hasse11,1978), temporal asynchrony between host and parasitoid populations (Griffiths,1969) or by host individuals varying in their defence against parasitism (Hassell and Anderson,1984). Hassell
(1984) concludes that 'with heterogeneity coming from so many sources, it is hard to escape the conclusion that it is a widespread mechanism contributing significantly to the stability of natural host-parasitoid interactions.'
The literature concerning the relevance of ecological theory to developing a general strategy for biological control has, in the main, been based on derivatives of the Nicholson-Bailey model (for example
Beddington, Free and Lawton,1978; Hasse11,1978,1980; May and Hassell,
1981) and it has been generally agreed that successful biological control results from the enemy imposing a low, stable host equilibrium.
Recently, Chesson (1978,1982), Murdoch (1979) and Murdoch, Chesson and
Chesson (1985) have challenged this view and have suggested that local pest extinction may be a more appropriate goal for biological control programmes. They explore this using stochastic, rather than deter- ministic, models and by introducing the concept of stochastic boundaries where the disturbance functions are given probability distributions. From such models the probability of a population being driven extinct may be established as well as the maximum probability that the economic threshold may be exceeded at any given time. Indeed,
Murdoch, Chesson and Chesson (1985) suggest that a stable pest equili- brium is neither a necessary nor a sufficient condition for control.
It is also pointed out that several deterministic models recommend parasitoid behaviour that stabilises by allowing a proportion of hosts - 220 - to escape parasitism, whereas stochastic models emphasise the para- sitoid's ability to drive the pest population as low as possible in any area, including to extinction.
Chesson (1978) commented that 'deterministic models may often be inadequate to model predator-prey interactions, stochasticity playing a fundamental role in such population processes.' The observed dynamic behaviour of real populations may, in fact, be explained by both deterministic and stochastic models. For example, populations that, in deterministic terms, appear to be tightly regulated around a fixed equilibrium point because of a constant environment, the ability to ignore environmental fluctuations or strong density dependence, will be narrowly 'bounded' in stochastic terms for similar reasons.
In attempting to detect regulatory processes it has been customary to plot some measure of proportionate mortality against population density. A statistically valid relationship indicates the presence of a density dependent process that may contribute to population stability.
Conventionally, a correlation between the 'k-value' for the mortality and the logarithm of the initial population density has been used. The
'killing power' or 'k-value' expresses logarithmically the effect of a mortality factor and is calculated as the difference between the
logarithms of the population before, N, and after, S, the mortality acts;
log10 k = (70 6.1
Varley and Gradwell (1970) and Bulmer (1975) have pointed out a major difficulty that arises from the use of k-values in exploring
potential regulatory processes. Density dependence should not be
accepted without questioning whether the regression of the k-value
for the mortality and the logarithm of the initial population is
significant as the variables of the regression are not independent. -221 -
The regression is given by
k = a + b log10 N 6.2
where b is the slope of the regression, a the intercept and N the
original number per unit area. When the independent variable is
population density, statistical tests for density dependency may
be invalid if fractional survivals, or logarithmic expressions of
these, are used as the dependent variable. Such tests are in
effect correlating (y/x) with or (log10 x - log 10 y) with log 10 x x and errors in the estimate of x can themselves result in an apparent
correlation between the two.
Varley and Gradwell (1968,1970) and Southwood (1978) have
expanded on the need to prove such a relationship where it is hoped
to produce a mathematical model which has biological meaning.
Varley and Gradwell (1968) argued that if both the initial and final
densities are determined from the same sample, as is the case when
measuring parasitism for example, a regression between the population
surviving the mortality (as the dependent variable) and the population
before the mortality (independent variable) on logarithmic axes provides
a valid proof of density dependency if the regression slope differs
significantly from a slope of b = 1. However, when the two measurements
of density are based on different samples, each subject to sampling
errors, this test is not valid as normal regression methods demand
that the independent variable is free from errors. In such cases one
possible proof of density dependence can be given if both the regres-
sions of initial density against final density and final density against
initial density produce slopes that differ significantly from a slope
of b = 1 and on the same side of this slope of unity. Difficulties are, however, known to arise from the use of this method. Bulmer (1975) - 222- argued that the existence of density dependent trends were often masked by temporal trends (i.e. delayed effects) in the data. In fact he found that even with a series of approximately 60 observations only strong density dependence was likely to be revealed. Southwood and
Reader (1976) were also unable to show any density dependence by this method in a 12 year census of populations of the Viburnum whitefly,
Aleurotrachelus jelinekii (Frauenf.) (Hemiptera:Aleyrodidae). Southwood
(1978) concluded that as the demonstration of density dependence was fraught with statistical difficulties, failure to detect it by this method in no way proved its absence.
An alternative regression technique when errors occur in both estimates is Bartlett's (1949) three-group method. In this procedure errors are equally apportioned between each axis by dividing the data pairs into three equal groups, or at least into two equally sized end groups.
Although various studies have been made of the mortality factors affecting the cabbage root fly a definitive study of density dependence, particularly on a spatial level within a generation, is lacking. The following experiment involves the planting of cohorts of various developmental stages of the cabbage root fly in the field, thus creating replicated differences in population densities from plant to plant. By doing this an attempt has been made to accurately pinpoint
the mortalities acting on the different developmental stages, to establish whether they have regulatory potential and to compare the results with laboratory observations (this study and P.M. Reader, unpublished data). - 223 -
6.2 A study to determine the effect of spatial heterogeneity on
mortality factors affecting cabbage root fly populations in
the field.
6.2.1 Materials and Methods.
Swede plants (8 - 10 weeks old) were transplanted into a fallow area of soil between two swede crops. The plants were inoculated with various densities (see Table 6.1) of cabbage root fly eggs, second instar larvae and pupae reared in the laboratory. All three develop- mental stages were placed on the soil surface around the swede plant and lightly covered with a thin layer of soil. They were left in the field for fixed periods of time (see Table 6.1) and subsequently collected and returned to the laboratory for classification and recording. The experiments were carried out from mid-June to mid-
September during both 1983 and 1984.
As in previous experiments (Chapter 5) it was necessary to obtain an estimate of the level of infestation that would arise over a 5 week period from the native cabbage root fly population. During both experimental periods swedes were transplanted and left for 35 days in the same area as the study swedes. In 1983, pupae were collected in the soil surrounding three of the thirty swedes used as controls.
Dissection of the swedes revealed a further five larvae. In 1984, six of the forty swedes had pupae in the surrounding soil, a further four containing larvae when dissected. While this may have affected results from individual swedes, it was again assumed that unbiased selection of host plants by the cabbage root flies, regardless of the level of experimental inoculation, ensured that overall results were not affected unduly. Host stage used to Interaction time Mortality factor Densities used inoculate plant (days) measured (per plant)
Egg 4 Egg 2 - 256
Egg 35 Total 4 - 128
Second instar larva 14 Larval 2 - 64
Pupa 7 Pupal 2 - 32
Table 6.1 Experimental details of studies used to
determine mortality levels at various
host development stages. Figure 6.1 a.) The density dependent relationship between the
initial density of cabbage root fly eggs (N) and
that remaining after 4 days in the soil (S).
Broken line indicates slope of unity (t-test for
significant deviation from b = 1, p < 0.05).
b.) As for a.) but in terms of k-value plotted
against initial density. Equation of line:
y = 0.075z + 0.054. - 226 -
2-5- a
2-0-
1-5- • • 1
05 / •3 I • 947/ • / 0-5 • /' • 4 I • .2. ,• / /
3 0 0-0 I 1 I I 1 0.0 0-5 1-0 1-5 2-0 2-5 Log ic, N.
0-5 - b. • • 0-4 - • • • • • • . 0-3 - • • • to z To • • > • • • 1 ..,...... /<• _t 0-2 - • • • • . ,00' • 0 • 2 • • • .2 • • • 4 • 2 • • • • • 0 -1- • • • • • • • • • • •7 04 • 0-0 1 1 f
0-0 0-5 1-0 1-5 2-0 2-5 Log ic, N. - 227 -
6. 2. 2 Results.
Egg mortality per se was not investigated during 1983. During
the summer of 1984 various numbers of eggs (see Table 6.1) were placed
around individual plants, those remaining after 4 days in the field being subsequently collected and counted. Practice runs in egg collec-
tion were made under laboratory conditions. A high proportion of eggs
(98 - 100 per cent) were returned by washing and egg loss arising from
collection was assumed to be negligible. The relationship between the
density of cabbage root fly eggs placed in the soil (N) and that sub-
sequently collected after four days (S) (Figure 6.1a.) yielded a slope
that differed significantly from unity. When k-value was plotted
against the logarithm of the population density (Figure 6.1b.), density
dependence was suspected as there was a significant deviation from a
line with zero slope. Since both densities were determined from the
same sample, the regression between log10 S and log10 N provided suffi-
cient proof of density dependence.
The responses obtained when various numbers of second instar
cabbage root fly larvae, ranging from 2 to 64 per plant, were left in
the field for 14 days have already been considered in the preceeding
Chapter (Experiment 5.2). The mortality observed in this case
(Figures 5.6 and 5.8) was assumed to be the combined effect of two
factors, that of larval disappearance, resulting from inability to
establish in host plants and predation by soil inhabiting arthropods,
and parasitism by T.rapae. While the initial number of larvae was
accurately known it was assumed that the larval population open to
parasitism by T.rapae was collected at the end of the experimental
period. It was, therefore, likely that, when considering parasitism,
both initial and final densities were subject to sampling errors. Con-
sequently, Bartlett's (1949) method was used to fit the regression line Figure 6.2 The density dependent relationships for larval
mortality from predation (a. and b.) and parasitism
by Trybliographa rapae (c. and d.). Solid line:
least squares regression (using Bartlett's (1949)
method for c. and d.); broken line indicates slope
of unity. All slopes differ significantly from
b = 1, (t-test, p < 0.05). Equation of lines are
as follows:
a.) y = 0.76x + 0.18
b.) y = 0.76x + 0.11
c.) y = 0.76x + 0.12
d.) y = 0.69x + 0.15. - 229 -
1983 1984
a. b. 2-0- - 0, / e / / „. , " 12 ' 1-5- ei_22f,-2 ,M.n e n • U) •e -3 9 1-0 - - a) e7710 0 I. _1 „.,,v•• Ir. I 0-5 - / / / ••• / . .Z./ I / e 0-0 I I 1 1 I 0-0 0-5 1-0 1-5 2-0 0 . 0 0-5 1-0 1.5 2-0
Log io N.
Larval predation.
C. d. 2-0 - / // / / • • 0 - eV 1-5 - • e / e:s• I ' el • .2 U) ./2" 410 00 • I • 2% 100. • • • • os, 2.15• • 1,2 , , n,••• 0 1-0- •••„. • m "rr . / •- o • • • •,•,•2 _I a.2 2 •404 8,P./ 6 • _4 0-5 - / •2 • • • e e / Xe; 4 .5 zn I • 0-0 ' • r 1 1 I I I I 0-0 0-5 1-0 1-5 2-0 0-0 0-5 1-0 1-5 2.0
109 10 N.
Larval parasitism. - 230 -
Figure 6.3 Density dependent mortality of larvae due to
factors other than parasitism. Equation of line
for a.) 1983: y= 0.243x - 0.176 and for
b.) 1984: y = 0.242x - 0.112. - 231 -
0-5-' a.
0-4 - • • • 2 0 • 0 -3 - • • / a, • 2 z 0 • > t ..tc 0-2 -n •
0 -1 -
0-0 • 0-0 0-5 20
0-5 b.
0-4 - •
0 -3 -
tiv 3 .- C0 2. I _v 0-2 -
3 0 • 0-1 - • • 2 0
7 .3 0-0 T • I 1 t 0•0 0-5 1-0 1 - 5 2-0
Log 10 N. Figure 6.4 Density dependent parasitism of Delia radio=
larvae by Trybliographa rapae. Equation of line
for a.) 1983: y 0.228x - 0.113 and for
b.) 1984: y = 0.312x - 0.153. - 233 -
0 -5 - a• • • 0 -4 -.
•
2 0 -1 --i
0-0 ...... 3 1 • .... I 1 0-0 0-5 1-0 1-5 2-0
109 10 N.
b. 0 -5-
0-4 -, •
• • / • • • • • 2 /2 2 • 0 -1 -.4
0-0 -r 3 .n 6 • -2 I I I 0-0 0-5 1-0 1-5 2-0
Log m N. - 234 - in Figure 6.2c. and d., a least-squares linear regression that only permits the y variable to be a random variable being less appropriate for these data. All the regression lines in Figure 6.2 suggest the existence of density dependent relationships and the data are plotted
in terms of k-values against the logarithm of the initial density in
Figures 6.3 and 6.4.
When pupae that had been left in the field for seven days were collected, pupal predation yielded density independent relationships in both 1983 and 1984 (Figure 6.5). As for T.rapae in the previous
Chapter, levels of parasitism were assumed to be represented by the proportion of the pupae collected after the experimental period parasitised by A.bilineata. In 1983, parasitism by the staphylinid did not exhibit any density dependence (Figure 6.6a.), levels of parasitism being negligible. The data from 1984 gave somewhat different results. Parasitism by A.bilineata yielded an inverse density dependent response (Figure 6.6b.) when k-values were plotted against the logarithm of the available host population. Proof of such a relationship was provided when the number of pupae surviving parasitism was plotted against the initial host number on logarithmic axes using Bartlett's method (see inset of Figure 6.6b.).
By placing various numbers of cabbage root fly eggs in the field and leaving them for 5 weeks an attempt was made to estimate the combined effect of a number of mortality factors. Six different mortalities were considered: egg mortality, including egg predation and inability of first instar cabbage root fly larvae to establish
themselves in a suitable host plant; larval predation; pupal predation; parasitism by T.rapae and A.bilineata and finally failure to emerge.
These 'killing factors' were referred to as k to k 6 respectively. Figure 6.5 Density independent predation of Delia radicum
pupae for a.) 1983 and b.) 1984. - 236 -
0-5- a.
0 -4-
•
0 -3- 02 0 3 • • 63 2 To > 1 At 0 -2- •
• 2
.2 •
0 -1 - • ,, 2
• •3 • • 2 0.0 4115+r. •5 • 72ir • • 2 e 0•0 0-5 1-0 1-5 2.0
Log,0 N.
0 .5- b.
0.4-
0-3-, • i 7 t7 2. • i At 0 .2- • 2 • • • • • 4 • 0 •4 • 3 • 3 • 0 . 1 - • •
0 2 • • • 2 7...... r. 3 0.0 • • • I I •
0•0 0.5 1 . 0 1.5 2.0
Log i° N. Figure 6. 6 Patterns of parasitism by Aleochara bilineata.
a.) 1983 - density independent, b.) 1984 - density
dependent relationship between mortality level,
given as k-values, and the potential host population.
(Equation of line: y - 0.179 - 0.099x. (Inset: the
density dependent relationship between the density of
host available for parasitism and those surviving
attack by Aleochara bilineata. Solid line: least
squares regression using Bartlett's (1949) method;
broken line indicates slope of unity.)) - 238 -
a. 0-5 -
0-4 -
0-3 - •
0-2 -
• 0 -1-
• • • 12 2 5 6 2 2 4 2 2 0-0 • Or • • • • VI 00 • •-• • 0111,• 0-0 0"5 1-0 1-5 2-0
Log io N.
b. 0-5- 1-5-
0-4 -
ADZ. • • •• • •• • 0-3 - 05 • 6/3 •
0-0 2 1 > 0-0 0-5 1-0 1-5 0-2 - • Log io N. 03
0 -1-
•••
4n 0 - 0 • • •• •r.• •-• •• 0-0 0-5 1-0 1-5 2-0
Log 10 N. - 239 -
The calculation of k-values for the latter three was relatively straight-forward and the relationships are shown graphically in terms of k-value plotted against the logarithm of the population density on which it acted in Figures 6.7 and 6.8 (d., e. and f.). Mortality due to failure of cabbage root fly to emerge from pupae was density indepen- dent for both years. This factor played a negligible role in the lower- ing of population levels. While parasitism by A.bilineata was density independent in 1983, an inversely density dependent relationship was initially suspected in 1984. This, however, proved not to be statis- tically significant. Parasitism by T.rapae yielded markedly directly density dependent patterns for both years. Using Bartlett's technique for linear regression when errors are suspected in both measurements, slopes differing significantly from unity were obtained when initial and final densities were plotted for a regression and correlation analysis of log10 S on log 10 N. These regressions were considered to provide valid proof for the existence of density dependent patterns of
parasitism.
When considered together, the summed effect of the remaining three
mortality factors for data from both years yielded density dependent
relationships that stood up to the appropriate statistical tests for
proving such patterns. The three factors could not be separated with-
out considering them in the light of previous experiments described in
this and the previous Chapter. Pupal predation, considered above,
yeilded density independent responses (Figure 6.5) in both years with
approximately 16 (1983) and 23 (1984) per cent of the pupae being
predated. As both the studies to measure total mortality and pupal
mortality were run concurrently, the level of predation recorded in
the earlier experiment was assumed to define that in the present set
of observations. Using this relationship the number of pupae prior Figure 6.7 The k-values for the different cabbage root fly
mortalities for 1983 plotted against the population
on which they acted. k i , k 2 and k 4 are directly
density dependent, k 3 , k5 and k 6 density independent.
(See text for details.) Line equations as follows:
a.) y = 0.55x - 0.25 0.485 -1 b.) derived from S = 1.384N (1 + (0.038N) )
d.) y = 0.19x - 0.02. 2 -0- • • • •8-2 a. 1-0 - 2 • ki • ....•*"'",1-4... 5 • :.--*''''1-5 • • , 2- 2 2 ...... /...... "...-1-- 1-3 6,,,...n 4 8 -2 0..3 0-0 1 : •-3 1 1 1
0 -2 - / 23 8 • i •3 #/y• b. 0-1- 4 ...... , 3•2 0 .0 --r•----- 11-10 -5-7 22 5 0'151 5 • 6 44 0'10 6 C. • 2 3•• 2 k3 3 2•2 Op,• •a 0-05 • •
111 3 0-00 ii s To 1 1 > I • ae 0-75 -
0-50 - • d. k4 3 • • n 0-25- c...•2 3.,,,2 %.,.z ' • 4...... •'-'• 2•8•L•o• 2 4 02 • • 0-00---1'-3 • ••
050]3 • • • 6 • •• e. 1(6 0-25 3 • ' 4 Ile • 2 . 5•3•3•• 3 3 4 62 . 0-00-p 8--n•-2 0-2—•
0'501 2 2 f. 0-25 2 • • k6 2 2 4 4 22, 00014___ 13__13 6.4 4 0-0 0-5 1-0 1-5
Log io N. Figure 6. 8 The k-values for the different cabbage root fly
mortalities for 1984 plotted against the population
densities on which they acted. k and k are directly 2 4 density dependent k k k and k density independent. 111 3, 5 6 Line equations as follows:
0.289 -1 b.) derived from S = 3.333N (1 + (7.737N) )
d.) y = 0.07x - 0.01.
- 243 -
0-501
2 • 2 3 2 • • a. 0-25 2 3 2 4 1-2 7 2 3 4 i • 2 3 • 0-00 I '• r r
0-501 . • 2 ....2t.- •2 • •••• b. 0-25 2 • 4 5 3 3 4- 2•"' 3' 0'00 r
0-2 1 8
4 23 45 2 2.•22 60. •.•3. • C. 0-1 3 3 4
0-0 3 I I I I
0-21 • 2 2 d. . 2 0-1 ••• ••: • • • • ....nr"...
• 2 2 I".No 0-0 '1-2r3 3- • -2 20-9 — • • 0-50 1
oe• 9 • • • e. 0.25 2 • •6 4 • • • • 3 3 0 . 00 -: 3 • .3._Si:.:.-, : • 0•21 • f. • 0-1 • • • 2 .4r • -ip 4--. 4 5 4..4..4—.42.•••2•2••---1 0-0 s s 0-0 0-5 1-0 F5
Log i° N. - 244 - to predation was estimated and k evaluated. By similar reasoning the 3 number of larvae predated was calculated from the relationship deter- mined in Experiment 5.2. Thus, k 2 and k l could be estimated, the number of eggs used in inoculating each swede plant being accurately known.
When 'egg mortality', k l , was considered, the data from 1983 yielded a statistically significant, directly density dependent, relationship while the data of 1984 showed complete independence from any density effect. This latter observation was not supported by earlier observations made of 'egg mortality' over four days
(Figure 6.1). The difference may have arisen in the way in which 'egg mortality' was defined in the present set of observations as including the inability of newly hatched cabbage root fly larvae to establish themselves in suitable host plants. In the earlier study mortality was restricted to egg predation.
Not surprisingly, the relationship between both k 3 and k 2 and the logarithm of population density showed considerable agreement with those already considered earlier in the Chapter. Pupal predation
(Figures 6.7c. and 6.8c.) was found to be density independent while larval predation yielded directly density dependent patterns of parasitism.
Linear regression was not found to provide the best description
of the relationship between the effect of predation on the larval
stage and the available larval population. Bellows (1981) found that
a model of density dependence, originally due to Maynard Smith and
Slatkin (1973), was well suited to describe a wide range of data.
Mathematically the model may be expressed as
S = d N (1 + N)8)-1 6.3
where S is the number of survivors and N the initial density. The
parameter d determines the level of density independent mortality - 245- while the density dependent form of the curve is determined by para- meters a and O. The parameter a is a scaling constant which determines, for a given value of 0, the density at which proportionate mortality reaches a fixed value, while the parameter 8 determines the severity of the density dependence. As well as being a more flexible and better descriptive form Bellows (1981) found this model to be less prone to over-estimates of density independent survival. Also, the model describes a relationship between k-value and log 10 N that is approxi- mately linear at high densities. As well as being appropriate for these present data (Figures 6.6b. and 6.7b.) such a relationship is also thought to play an important data describing role by Varley, Gradwell and Hassell (1973), Hassell (1975) and Stubbs (1977).
6.2.3 Discussion.
The importance of detecting the presence of density dependent processes acting within a population is unquestionable. This is particularly true when attempting to establish the existence of any factors (for example, natural enemies) that may contribute significantly to population regulation for a pest management programme. Various studies have been made of the population dynamics of the cabbage root fly. Hughes and Salter (1959), in exploring five years' records of the population losses occurring during the first generation of the cabbage root fly, found that egg mortality was the most important.
However, they made no attempt to study its regulating ability. Hughes and Mitchell (1960), in a more accurate, detailed study constructed life-tables for six generations of the pest as it occurred at N.V.R.S.,
Wellesbourne. They concluded that whilst cabbage root fly populations had remained 'remarkably' constant over the years, no particular factor seemed to be concerned in this regulation. They suggested - 246 - that varying combinations of all factors, possibly modified by weather conditions, seemed to be able to cope with any potential increase or decrease in numbers before the end of the generation in which the change occurred.
Mukerji (1971) analysed life-table data for nine generations at
two locations in Ontario and showed that extensive mortalities occurred during the following age intervals: (1.) egg stage, (2.) between hatching and the second moult, (3.) third instar larvae and (4.) pupal stage. Analysis of age interval survival and graphical key- factor analysis showed that 'misadventure' of the larvae between hatching and the second moult was the key factor. Mukerji also found that while the overall mortality process from egg to adult eclosion was density dependent, density dependent mortality occurred only during the pupal stage. Thus he considered pupal parasitism to be of considerable importance as a stabilising factor. Prompted by this study Benson (1973) re-analysed and re-interpreted both Mukerji's
(1971) Canadian data and Hughes and Mitchell's (1960) English fly population data. He found pupal mortality to be density dependent in both populations. In Canada this was caused by parasitoids and predators, especially the parasitic staphylinid A.bilineata, while predatory staphylinids and carabids were believed to be the main agents of regulation in England.
Egg mortality was the most important factor lowering population levels in the present study and there was a strong suggestion
(Figures 6.7 and 6.8) that this factor may have the greatest regulatory potential. Predation of cabbage root fly eggs yielded both directly density dependent and density independent relationships. Hughes (1959)
lists eight staphylinid and carabid species that are particularly
ready feeders on the egg stage of the cabbage root fly. At N.V.R.S., - 247 -
Wellesbourne where the study was carried out, Bembidion lampros (Hbst.),
Trechusquadristriatus (Shrank) (Coleoptera:Carabidae) and Aleochara bipustualta were the only species present in sufficient numbers to be considered of any great importance. Estimates made by Hughes showed that egg predation was the major cause of egg mortality, accounting for over 90 per cent of the losses in the first generation. However, no attempt was made to establish whether there was any heterogeneity in the levels of parasitism from plant to plant. Wright, Hughes and
Worrall (1960) found that there was an inverse relationship between egg survival and the numbers of B.lampros caught in pitfall traps placed near cauliflower plants. Coaker and Williams (1963) showed that, by excluding adult beetles from experimental plots, carabid beetles were responsible for about one-third of the egg mortality while
Coaker (1965) suggested that about two-thirds of the total mortality of cabbage root fly populations occurred at the egg stage. Mowat and
Martin (1981), in estimating the contribution of predatory beetles
(Carabidae and Staphylinidae) to the control of cabbage root fly populations in transplanted cauliflowers, found the contribution of staphylinids difficult to evaluate but considered carabids to be the more significant predators. They argued that B.lampros, assisted by other Bembidion species, probably accounted for most of the egg pre- dation (> 50 per cent of the eggs laid) which was observed.
Total egg predation over the various densities in the present study ranged from 27.5 to 50.6 per cent. Recent work by S. Finch
(pers.comm.) at N.V.R.S., Wellesbourne found similar levels of preda- tion (approximately 40 per cent) on samples of 100 eggs placed around individual plants.
Larval predation and parasitism were also found to exhibit density dependence and, as a result, had a regulatory potential. - 248 -
Hughes and Mitchell (1960) found a similar pattern between percentage larval parasitism by T.rapae and host density between generations but the relationship was not significant. In this latter case the rate of parasitism only doubled over a four fold increase in host density and
Hughes and Mitchell considered it unlikely that this mechanism could have any important stabilising effect on population numbers. When considering the regulatory potential of any factor it must be noted that if a density dependent effect is not operative under all conditions, or is one of anumber of density dependent factors acting on a population, individually each factor may be incapable of regulating the population.
It is clear that how density dependent relationships are detected in the field is critically important in drawing any conclusion regard- ing their regulatory potential. The detection of natural enemies, in particular, as density dependent factors is difficult, especially when they act together with other stochastic processes. Hassell (1985) has conclusively shown that the main difficulty lies in attempting to detect density dependence that arises within a generation by non-random para- sitism between patches of different host densities from estimates of mean population size per generation. The only real solution to the problem is to seek more detailed information, as in the observations above, of levels of parasitism, or predation, within each generation.
This may often prove not only time-consuming and laborious, but also difficult if, for example, generations overlap as in the cabbage root fly. However, it is essential that some experimental and sampling regime is developed that takes the dimensions of space as well as time into consideration. Otherwise, as Hassell states 'there is the very real risk of failing to identify the true reasons for the relative stability of many natural populations.' - 249 -
It was established in Chapter 5 that there was considerable
qualitative agreement between laboratory and field observations on
the pattern of parasitism exhibited by T.rapae. While quantitatively different, the general density dependent pattern of parasitism was unquestionably present under both conditions. This conclusion is further supported by the observations made in the present Chapter.
Laboratory studies of the foraging behaviour of Aleochara bitineata have indicated the presence of density independent and inversely density dependent patterns of parasitism (P.M. Reader, unpublished
data) of D.radicum pupae. The value of such observations are
strengthened by the patterns of parasitism observed in the comparable field studies (Figure 6.6).
Laboratory experiments, as well as providing an insight into the resulting distribution of parasitism, also enable the behavioural aspects that give rise to such patterns to be studied. The aggregative response of T.rapae has already been discussed in some detail earlier
in this study and P.M. Reader (pers.comm) has found that the foraging behaviour and functional response of A.bilineata provide possible explanations of the level and pattern of parasitism exhibited by this beetle. Similarly, Mitchell (pers.comm. to Hughes (1959)) found that the locomotory behaviour of both Bembidion sp. and Trechus sp. indivi- duals changed after they had eaten an egg of D.radicum. The predators no longer moved in more or less straight lines but, for a period of several seconds, appeared to perform a series of tight turns before they resumed normal motion. This behaviour, comparable to the examples of klinokinesis described in Chapter 2 for various parasitoid species, usually meant that any nearby eggs were quickly located. In laboratory experiments, once a group of eggs was discovered, the beetle usually remained there until the number of eggs in the group was so reduced - 250 -
that even the turning movements were unlikely to increase the chance of contact. Such behaviour could well give rise to density dependent • patterns of predation similar to those in Figures 6.1 and 6.7.
While this study has gone some way in exploring and determining the factors that affect and regulate cabbage root fly populations, certain contradictions, such as the importance of pupal mortality from predation as a regulatory factor (Benson, 1973; this study), still remain unsolved. There is still an obvious need for a long- term, definitive study of the mortality factors affecting the cabbage root fly on both a temporal (inter-generation) and spatial (intra- generation) level. -251 -
CHAPTER 7
GENERAL DISCUSSION AND CONCLUSIONS
The identification and exploration of the essential components
of the population dynamics of both host-parasitoid and predator-prey
interactions under field conditions is not easily undertaken.
Consequently, although a number of detailed, long-term, field
population studies (see Chapter 5 for examples) and shorter laboratory
observations (see Hasse11,1978) are recorded in the literature, there
are few studies where field and laboratory observations have been
made with the intention of establishing how accurate are laboratory
investigations on the components of host-parasitoid population
dynamics when compared with what happens under field conditions. The
lack of such studies has given rise to various criticisms, and certain
workers (for example, Dempster,1975) have argued that only limited
progress is possible in the construction of realistic population
models on such a basis. This study has been concerned with the
patterns of parasitism shown by the cynipid Trybliographa rapae on
populations of the cabbage root fly, Delia radicum, a major pest of
cruciferous crops in Britain. As natural populations occur in abun-
dance in untreated cruciferous crops, and laboratory cultures can be
established and maintained with relative ease, the interaction has
provided a rare opportunity to study levels of parasitism under both
laboratory and field conditions.
Trybliographa rapae was able to parasitise the three instars of
its host, the cabbage root fly, D.radicum, but showed a marked
preference for the first two instars. Under natural conditions the younger larvae are far more likely to be parasitised as they are more readily accessible. From the laboratory observations made during this - 252- study the rate of oviposition, even when the parasitoid was presented with excess hosts, was low, seldom exceeding more than 8 to 10 hosts being parasitised per 48 hours. The low rate of oviposition by T.rapae may have been associated with the fact that locating potential hosts burrowing in Brassica tissue is not only time consuming but difficult,
although the parasitoid has been found burrowing to considerable depths within the host-plant tissues. Price (1975) commented that parasitoids
attacking more abundant host species tended to have a higher fecundity
than parasitoids of less abundant host populations. The relatively low
fecundity of T.rapae (ranging from 4 to 80 eggs for females living 2 to
24 days respectively) as compared to other parasitoids (for example,
the ichneumonid Itoplectis conquisitor (Say.) has a fecundity of about
300 eggs (Leius,1961) while the gregarious parasitoid Nasonia vitri-
pennis produces up to 820 progeny per female (Nagel and Pimente1,1963))
may be associated with the somewhat dispersed pattern of cabbage root
fly popluations.
Aspects of host location by various parasitoid species has received
considerable attention (for examples see reviews by Hassell and South-
wood,1978; Waage,1977; Vinson,1984a. and b.). The majority of workers
believe that the environment is perceived by the foraging individual
at several hierarchial levels. When olfactory responses are studied,
it is important to determine which of these levels are actually being
considered. Trybliographa rapae was found to show a marked preference,
within a 'choice-chamber', for areas from which strong Brassica odours
were emanating. There are numerous examples in the literature, some
of which are cited in Chapter 2, illustrating that chemostimulants are
commonly used for host-habitat location by parasitoids. Although it
must be stressed that experiments of the kind described in this study
cannot be used to determine whether the parasitoid is attracted
(sensu. Waage,1978) by such chemicals, the results support the - 253 -
findings of other workers (L.Vet, pers.comm.) that T.rapae uses
chemicals emanating from the host plant to locate the habitat of
potential hosts.
A combination of host frass and changes in the host medium arising
from the presence of the cabbage root fly larvae is believed to have
resulted in an arrestment response (sensu. Dethier, Browne and Smith,
1960) on areas where potential hosts could be found. Trybliographa
rapae exhibited both an orthokinetic response to the presentation of
stimulus which involved stopping, walking slower and increasing the
level of probing, and a directed, klinotactic response that turned the
wasp back onto the area on which it was foraging. In a recent review
of host location by parasitoids, Vinson (1984a.) concluded that para-
sitoids practice a 'form of espionage' on the lives of their hosts.
He argued that by evolving responses not only to their hosts, but to
stimuli emanating from organisms associated with their hosts' food or
shelter, parasitoids are, in fact, exploiting the requirements of hosts
to communicate intra-specifically, feed and defend themselves.
The avoidance of superparasitism is generally of considerable
selective value to solitary parasitoids, particularly so when the
number of eggs or the duration of handling time are limiting factors.
This apparent restraint in oviposition on the part of the searching
female, even when hosts are scarce, provides the progeny with a maximal
chance of survival. Although not exhaustive, results from the present
investigation suggested that the ability of a T.rapae female to detect prior parasitism and avoid subsequent superparasitism depended on whether or not it laid the first egg. During the 48 hours subsequent to an oviposition superparasitism was more likely to occur when wasps encountered hosts containing eggs that were not their own than when they re-located hosts previously parasitised by themselves. After this - 254 - period superparasitism was avoided to a considerable degree under both conditions. After oviposition, parasitoid eggs require 96 hours before hatching. If an egg is laid within this period in a host already parasitised by a conspecific there is a chance, albeit small, of the second egg supplanting the first. Studies showing such patterns in the solitary parasitic wasps are rare in the literature; the majority show some avoidance of superparasitism regardless of whether the wasp laid the first egg. Bakker et (1/.(1985) have, however, recently argued that although there is little indication that marks are individual there
is no reason to suppose that conspecifics would avoid superparasitising
if it would be advantageous for them so to do.
On locating potential hosts the efficiency of the parasitoid in
parasitising individuals is of obvious importance. This may be measured
in various ways, the classical method of determining how the rate of
parasitism is influenced by prey availability being the functional
response of Solomon (1949). How applicable such responses are to
natural conditions is uncertain but such observations enable detailed
comparisons of searching efficiencies under various conditions. For
the T.rapae - D.radicum interaction explored in this study the
functional response was found to be best described, regardless of host
instar or host plant used, by a special case of the Hassell, Lawton
and Beddington (1977) model for describing Holling's (1959a.) Type 3
response. It was assumed that searching efficiency was directly
proportional to the host numbers present in the area being searched.
Only relatively recently have Type 3 responses been found to describe
invertebrate interactions, but the increasing frequency with which they
occur in the literature suggest that they may be more prevalent than
previously thought. - 255-
Of the three forms of functional response described by Holling
(1959a.), it is only the Type 3 response that is capable of having a potentially stabilising effect on the host-parasitoid interaction.
While Hassell and Comins (1978) have shown that such a response cannot,
on its own, stabilise a difference model, Nunney (1980) has argued that
in a model where the parasitoid can discriminate between parasitised and
unparasitised hosts the sigmoid functional response does have a stabi-
lising effect. Whether a Type 3 response has a significant stabilising
influence in the field is uncertain but the presence of such a response
adds to the likelihood of stability when other density dependent factors
act on the system.
Parameter estimates indicated that a longer period of time was
required to 'handle' a third instar larva than the two younger instars
probably a consequence of the thicker larval skin of the former. A
similar pattern was also apparent when the searching efficiency para-
meter b from Equation 3.22 was considered. The slightly higher value
of b for second instars was thought to be the consequence of these
larvae being easier to locate and attack because of their larger size.
When standardised hosts were presented on different plants, the
various estimates of handling time showed no differences. The attack
rate was, however, lower on both swede disc and radish than on the
Brussels sprouts plant, the difference thought to be the consequence
of plant structure. This factor has also been considered of importance
in determining the quality of a host-containing habitat by other
workers (for example, Carter, Sutherland and Dixon,1984; Gardner and
Dixon,1985).
Under natural conditions a host-parasitoid interaction will be
characterised by parasitoid individuals being faced with a range of
host developmental stages. Having an adequate description of the - 256 - functional response curves when instars are presented separately does not allow a realistic prediction of the consequence of presenting mixed populations. When more than one host 'type' is available parasitoids may 'switch' from one host category to another as their relative abundance changes. Trybliographa rapae failed to exhibit any preference for either first or second instars but showed active rejection of the third instar when presented in mixed populations. On the basis of the
individual functional responses a switching response was predicted when
first and second cabbage root fly instars were presented together, with
the most abundant host being attacked supra-proportionally. Murdoch
(1977) predicted that a general predator spending a disproportionate
fraction of search time in an area as the relative prey abundance there
increases also causes switching, changing a functional response from
one that imposes a risk on the average prey that decreases with prey
density in the direction of one that imposes an increasing risk. Such
switching repsonses are known to have a stabilising potential but as
Murdoch (1977) states, while a switching predator may help stabilise
one or more of its prey 'types' it may have relatively little effect on
the predator's stability or on total prey density. Experimentally,
however, the proportion of each host attacked was found to be directly
related to its relative abundance in the environment. It may be that
the parasitoid did not recognise the population as comprising of two
host categories, this resulting in similar levels of parasitism to
those obtained when each instar was presented separately.
Although crucial for the prediction of the effects of parasitism
on population dynamics and the rate at which these effects take place,
the relevance of laboratory derived functional responses in nature has
been questioned. Putman and Wratten (1984) have described them as
'ecologically primitive' as they are formulated on a system where - 257 - parasitoid individuals search at random for a fixed density of randomly arranged hosts. In the field situation a parasitoid will move between areas which contain hosts at different densities and a single parasi- toid confined within a small arena with uniformly sized hosts appears somewhat meaningless under such conditions.
When presented with a heterogeneous host environment, T.rapae exhibited a marked aggregative response, spending a higher proportion of its foraging time in areas where potential hosts were plentiful.
Possible behavioural patterns leading to such a phenomenon have been considered in Chapter 4. This aggregation of parasitoids where hosts
are abundant provides a potentially powerful stabilising mechanism for
host-parasitoid interactions (Hassell and May,1973,1974; Murdoch and
Oaten,1975; Murdoch,1977; Hasse11,1978). Most herbivores, predators
and parasitoids appear capable of exhibiting such an aggregative
response, concentrating their attacks on a particular portion or patch
of the resource. Any tendency to stabilise the interaction arises from
the provision of a partial refuge for the resource (host,prey etc.).
Hassell (1978) considers the relative importance of two types of
refuge: those where a constant proportion of prey are protected from
generation to generation, and those where a constant number are
protected. Both are potential stabilising mechanisms, the 'constant
number' refuge being the more significant.
An aggregative response was recorded at the five densities of
T.rapae used in the experimental studies described. At low parasitoid
densities there was no difference in patch-time allocation during the
initial hours of the experiment. Subsequently, there was a marked
selection for the patch with the highest host density, the females
spending most of their foraging time on this area. Increasing para-
sitoid density resulted in a higher proportion of searching time being - 258 - allocated to patches other than the high density ones, particularly in the closing hours of the observations. Thus, patches where the para- sitoid's rate of encounter with potential hosts had been lowered were left, the wasp moving to areas where there was a higher, or at least equal, likelihood of finding potential hosts.
This tendency of T.rapae to aggregate, and spend more time in patches where cabbage root fly larvae were more plentiful, increased the likelihood of encounter with one another and with previously parasitised hosts than if they had been distributed randomly. This
'likelihood of encounter' and subsequent interference increases with parasitoid density and has the potential of reducing the time available for T.rapae to forage for hosts. By using Hassell and Varley's (1969) method of demonstrating the existence of such interference, the total interference level observed was partitioned into mutual interference
(i.e. behavioural) and pseudo-interference (sensu. Free, Beddington and Lawton,1977). Actual behavioural interference accounted for
11 per cent of the total level, with the effect of non-random parasi- tism (pseudo-interference) explaining a further 28 per cent. More than half of the remaining interference could be explained by the increased level of superparasitism at high parasitoid densities. This observa- tion lends support to the earlier finding that female T.rapae are unable to differentiate between healthy hosts and hosts parasitised by conspecifics. Any remaining interference was assumed to have arisen from intra-patch interference which was not recorded in the present study.
The consequence of such interference (both mutual interference and pseudo-interference) among parasitoid individuals is a density depen- dent reduction in the rate of attack per parasitoid and thus, it is assumed, a density dependent reduction in parasitoid fitness. - 259 -
Hassell (1978) argued that the balance between the processes of
aggregation and interference should result in an optimal parasitoid
distribution at any given time. Such a concept had previously been
developed by Fretwell and Lucas (1970) into the 'ideal free distri-
bution' discussed in Chapter 4. There appears to be a complex and
dynamic interaction between aggregation (pseudo-interference) and
behavioural interference. In a natural situation, mutual interference,
if it occurs, increases with an increased tendency to aggregate as
this, by definition, leads to a higher probability of encounter.
The general overall effect of mutual interference will be to drive
parasitoid individuals from dense aggregates which will tend to
reduce the level of aggregation, and ultimately reduce mutual
interference itself. Both aggregative behaviour and mutual parasitoid
interference represent strategies adopted by parasitoids (and predators
in general) to increase their own fitness.
The literature contains numerous reports of the patterns of
parasitism within a heterogeneous environment where hosts exhibit a
clumped distribution among units of their habitat (see Hasse11,1978
for examples). There are considerably fewer studies (see Chapter 4)
where parasitoids have been presented with an environment where hosts
are distributed equally among sections of the habitat. The experiments
described in Section 4.4 made an attempt to establish how patterns of
parasitism by T.rapae on D.radicum would differ when the cynipid was presented with such an environment from that obtained when hosts were aggregated.
More hosts were parasitised by T.rapae when they (the hosts) were distributed in an aggregated manner. Aggregation led to higher rates of searching than random, non-directed search. However, at high parasitoid densities the profitability of continual aggregation fell - 260 - as host areas were exploited and a more even search strategy became as, if not more, preferrable.
The total level of interference, as measured by m, the coefficient of interference, when hosts were distributed equally among patches was not significantly different from that when hosts were aggregated.
However, the relative contribution of the component parts of inter- ference (mutual interference and pseudo-interference) differed significantly to those already described for the heterogeneous environment. Behavioural interference explained approximately a quarter of the total interference, with pseudo-interference explaining the remainder. The presence of pseudo-interference when hosts were distributed equally among the five patches was explained by the observation that, although no preference was shown overall for any particular patch, each replicate resulted in certain host areas being exploited more than others. When each patch was considered individually such inter-patch differences were of obvious importance.
When hosts were distributed in an aggregated manner significantly higher levels of superparasitism occurred at the two highest parasitoid densities. There was no such difference between levels of super- parasitism at various parasitoid densities when hosts were distributed equally between patches. While superparasitism was found to be important under conditions of host aggregation and high parasitoid densities in the laboratory whether a similar pattern would occur under natural conditions is doubtful, the likelihood of such parasitoid aggregation being very low.
The use and value of laboratory studies to predict what happens under field conditions has received considerable attention over the last decade (for example, Dempster,1975; Diamond,1983; Hasse11,1978,
1982c., 1985). Although laboratory studies are carried out in closed, -261 -
constant systems, by eliminating many of the vagaries of the field
situation the outcome of natural interactions may be more simply
classified and predicted. Naturally occurring cabbage root fly
populations were found in aggregated distributions, with the number
of pupae around a single plant only occasionally exceeding the highest
density in the laboratory experiments. Thus, it was hoped that the
patterns of parasitism by T.rapae observed in the laboratory arenas
represented, to some degree, those found to occur in the field.
Laboratory, field and natural experiments showed that a density
dependent response, where a higher proportion of cabbage root fly
larvae was parasitised by T.rapae where they were most dense, was
characteristic of the host-parasitoid interaction being studied.
Morrison and Strong (1980) have argued that most parasitoids do not
generate such positive spatial density dependent patterns of parasitism
in the field. Lessells (1985) however, in a study of the spatial dis-
tribution of parasitism by insect parasitoids showed that of 41 field
examples, 14 showed density dependent parasitism per patch, 14 showed
inverse relationships, two yielded 'domed' relationships and a further
11 were density independent. Within the field cages the overall level
of parasitism was higher than in the laboratory, probably the direct
consequence of the longer experimental period. More striking was the observation that the low host density patches were exploited to a higher degree in the field than in the laboratory. The lack of any significant difference in the mean number of eggs per parasitised host at the four parasitoid densities used in the field indicated the presence of either a strong tendency to disperse from the high density host patches at high parasitoid densities, or a reduced aggregative response arising from a weakening of the chemical stimuli emanating per unit area from the experimental swedes. - 262-
Searching efficiency in the field was considerably lower than in
the comparable laboratory observations. This was to be expected since,
as well as no consideration being given to the areas of the two
different arenas, whole swede plants presented the foraging parasitoid
with a more multi-dimensional area to forage on. The level of inter-
ference was also lower in the field; a probable consequence of the
less marked differential exploitation of host patches at high parasitoid
densities, the aggregative response of T.rapae being not as strong under
field conditions as in the laboratory arena. However, although the
degree of differential exploitation of infested areas and resulting
interference among individual foragers may have been less pronounced
in the field than in the laboratory, the general pattern of density
dependent parasitism was undoubtedly present under both conditions.
Various workers have considered the importance of density depen- dence as a regulatory factor in population dynamics. Nicholson (1933,
1954,1957,1958) argued that density dependent interactions played a major role in regulating population size while Andrewartha and Birch
(1954) took the view that density dependent processes were of only minor importance in determining the abundance of certain species.
Milne (1957a.,b., 1962) believed that the latter authors under- estimated the part played by density related processes in the deter- mination of animal numbers but, at the same time, thought that Nicholson had over-estimated the frequency with which intra-specific competition occurred in nature. Milne argued that, for the most part, control of population increase is due to the combined action of density independent and imperfectly density dependent environmental factors. Later workers
(for example, Southwood and Comins,1976; Hasse11,1978; Strong, Lawton and Southwood,1984) have illustrated the importance of natural enemies in the regulation of insect populations although certain authors (for example, Dempster,1983) have challenged this view. - 263 -
Density dependent processes are widely assumed to be necessary as
a means of regulating population size. However, while all density
dependent effects do share a tendency to regulate populations, if a
density dependent effect is not operative at all densities, or is not
operative under all environmental conditions, is weak, or happens after
some time delay, then the effect, although density dependent, may not actually regulate population levels. Similarly, if there are several density dependent factors acting on a population, while together they may regulate the population each factor on its own may be incapable of doing so. Although it was not intended to study the regulation of cabbage root fly populations as such, having determined that parasitism by T.rapae exhibited density dependence and thus had a regulatory poten- tial it was considered of value to determine whether any other mortality factors showed similar patterns.
Both egg mortality, arising from predation by staphylinid and carabid beetles, and larval predation were found to be density dependent while pupal predation yielded a density independent relationship.
Parasitism by Aleochara bilineata, a staphylinid predator and parasitoid, yielded both density independent and inverse density dependent responses.
Recent work has illustrated that these latter responses may also have a potentially regulatory effect on populations (Hasse11,1984). Failure of adult cabbage root flies to emerge from the puparia was negligible and density independent.
A brief study of multiparasitism of D.radicum by T.rapae and
A.bilineata revealed that, in cases of multiparasitism, A.bilineata developed if the staphylinid larva entered the puparium before the
T.rapae larva changed from its endoparasitic to its ectoparasitic stage.
If multiparasitism occurred during the latter stage it was the cynipid that was successful. Multiparasitism, particularly while T.rapae was - 264 - in its endoparasitic stage, also resulted in higher levels of mortality with no insects emerging from the puparium. Whether this was the result of a scramble type interaction with neither parasitoid obtaining sufficient nutrient to complete development was not established.
Experimental observations similar to those described in this study have resulted in the accumulation of a considerable empirical base.
From such a base the effects of predation (including parasitism) on the population dynamics of interacting species have been modelled, and predictions have been made on the overall dynamics of interacting populations and the outcome of biological control programmes. For example, on the basis of models based on laboratory systems, Hassell
(1978) argued that an ideal parasitoid for biological control in a perennial crop system would be one with a high search rate, promoting low equilibrium host populations, and a marked ability to aggregate in patches of high host density, thus stabilising the equilibrium.
As mentioned above, the use of such laboratory based models in predicting what would have happened under natural conditions has been criticised. This study has, to some degree, considered this argument using a host-parasitoid interaction that has enabled comparable field and laboratory studies to be made. As discussed, there was considerable qualitative agreement between the pattern of parasitism by T.rapae observed under experimental (laboratory and field) and natural conditions.
The occurrence of a similar density dependent pattern under all three conditions makes it difficult to escape the conclusion that such a mechanism is a real feature of the system and may have the potential to contribute to the stability of the natural host-parasitoid interaction.
Agreement, as observed in this study, between conclusions tested by different methods undoubtedly make the argument considerably more robust and potentially more useful. - 265 -
Finally, there is a definite need for further studies on the factors regulating cabbage root fly populations. As a major pest of
Crucifers an effective management programme should be based around any factors that may contribute significantly to its regulation. Past studies (for example, Hughes and Mitche11,1960; Mukerji,1971; Benson,
1973) have been based on average populations per generation, any density dependent mortality on a spatial scale within generation (for example, from plant to plant) may well have gone undetected. While this present study has briefly touched on this issue (Chapter 6), both intra- and inter-generation processes need to be explored in more detail in the form of life-table data stratified both in space and time. It is only by such analyses that the true causes of population regulation will be detected. - 266 -
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APPENDIX 1
The natural enemies of Delia radicum.
The following list is based on a survey of the Review of Applied
Entomology, Volumes 1 - 73.
Hymenoptera.
1. Ichneumonidae.
Atractodes gravidus (Gray.) Adashkevich,1983 Atractodes tenebricosus (Gray.) Wadsworth, 1915 Hemiteles ruficoxus (Prov.) Gibson and Treherne,1916 Phygadeuon detestator (Thubl.) Adashkevich,1983 Phygadeuon dimidiatus (Thorns.) Adashkevich,1983 Phygadeuon fumator (Gray.) Wadsworth, 1915 Phygadeuon trichops (Thorns.) Wishart,Colhoun and Monteith,1957 Stilpnus gagates (Gray.) Meyer,1927;Vodinskaya,1928
2. Braconidae.
Alysia manducator (Panz.) Paillot,1914 Alysia ruficeps (Nees.) Paillot,1914 Aphaereta auripes (Prov.) Wishart,1957 Aphaereta difficilis (Nees.) Nixon, 1939 Aphaereta minuta (Nees.) Brdmond,1937 Aphaereta tennuicornis (Nix.) Wishart,Colhoun and Monteith, 1957 Docnusa stramineipes (Hal.) Smith,1927a.;Lundblad,1933 Edcnusa thysa (Nic.) Adashkevich,1983 Microgaster anthomyiarum (Bch.) Paillot,1914 Opius procerus (Wesm.) Paillot,1914;Picard,1930 Opius spinaciae (Thorns.) Adashkevich,1983 Pentapleura fuliginosae (Hal.) Adashkevich,1983 Phaenocarpa pegomyiae (Brues.) Fischer,1973 Risarcha pubescens (Curt.) Adashkevich,1983 Taphaeus conformis (Nees.) Schutze and Roman,1931; de Wilde,1947a.
3. Eucoilidae.
Cothonaspis gerasimovi (Meyer.) Meyer, 1926 Eueoila spinosa (Htg.) Vasina,1927 Trybliographa rapae (Westw.) Westwood p 1835;Du Porte,1913; Gibson and Treherne,1916 Trybliographa gerasimovi (Meyer.) Meyer, 1927 - 294 -
4. Figitidae.
Figites anthomyiarum (Belie.) Paillot,1914
5. Pteromalidae.
Pdchycrepoideus dubius (Ashm.) Gibson and Treherne,1916 Spatangia nigra (Lat.) Bromand,pers.comm.
6. Diapriidae.
Loxotropa tritoma (Thorns.) Wishart,Colhoun and ?4onteith,1957 Trichopria cilipes (Kieff.) Adashkevich,1983
7. Formicidae.
Formica fusca (L.) Schoene,1916 Solenopsis molesta (Say.) Schoene,1916 Lasius niger (L.) Schoene,1916
Diptera.
1. Anthomyiidae.
Coenosis flavifrons (Stein.) Schoene,1916
2. Scathophagidae (Scatophagidae).
Scatophaga stercoraria (L.) Read,1958
3. Muscidae.
Muscina assimilis (F11.) Adashkevich,1983 litddea duplicata (Mg.) Vodinskaya,1928 Phaonia trimaculata (Bch.) Smith, 1927b.
Coleoptera.
1. Staphylinidae.
Aleochara bilineata (Gyn.) Wadsworth,1915 Aleochara bipustutata (L.) Schoene,1916;de Wilde, 1947b. Dinaraea angustula (Gy11.) Gibson and Treherne,1916 Hesperobium ca1ifornicum (Lec.) Gibson and Treherne,1916 Leptacinus batychrus (Gy11.) Adashkevich,1983 Orus punctatus (Casey.) Gibson and Treherne,1916 Omytelus insecatus (Gray.) Adashkevich,1983 Omytelus rugosus (Cray.) Adashkevich,1983 Paederus fuscipes (Curt.) Adashkevich,1983 - 295 -
1 Staphylinidae. (continued)
Philontus addendus (Sar.) Adashkevich,1983 Philontus concinnus (Gray.) Adashkevich,1983 Philontus decorus (Gray.) Adashkevich,1983 Philontus fuscipennis (Mann.) Adashkevich,1983 Philontus quisquilarius (Gyn.) Adashkevich,1983 Philontus rectangulus (Sharp.) Adashkevich,1983 Philontus sordidus (Gray.) Adashkevich,1983 Quedius ochripennis (Men.) Adashkevich,1983 Stenistordes cephatotes (Hr.) Adashkevich,1983 Stenus biguttatus (Z.) Adashkevich,1983 Tachyporus hypnorum (F.) Adashkevich,1983 Tachyporus nitidulus (F.) Adashkevich,1983 Xantholinus gtabaratus (Gray.) Hughes, 1959 Xantholinus harnatus (Say.) Gibson and Treherne,1916
2. Carabidae.
Acupalpus meridianus (L.) Adashkevich,1983 Acupalpus suturalis (De].) Adashkevich,1983 Agonum dorsale (Pont.) Mowat and Martin,1981 Anisodactylus signatus (Pz.) Adashkevich,1983 Amara aenea (Deg.) Adashkevich,1983 Amara convexiuscula (Msch.) Adashkevich,1983 Amara ingenua (Duft.) Adashkevich,1983 Amara similata (Gyn.) Adashkevich,1983 Brachinus crepitans (L.) Adashkevich,1983 Bembidion lampron (Hbst.) Hughes, 1959 Bembidion litorale (Olivier.) Hughes,1959 Bembidion mutatum (G. & H.) Gibson and Treherne,1916 Bembidion properan (Steph.) Adashkevich,1983 Bembidion quadrimaculatum (L.) Hughes,1959 Bembidion quadripustulatum (Serv.) Adashkevich,1983 Bembidion trechiforme (Lec.) Gibson and Treherne,1916 Calathus halensis (Schall.) Adashkevich,1983 Clivina fossor (L.) Adashkevich,1983 Harpalus distinguendus (Duft.) Adashkevich,1983 Harpalus hespes (Stern.) Adashkevich,1983 Barpalus tardus (Pz.) Adashkevich,1983 Microlestes negrita (Woll.) Adashkevich,1983 lificrolestes minutulus (Cz.) Adashkevich,1983 Nebria brevicollis (F.) Ryan and Ryan,1980 Ophonus rufipes (Dej.) Adashkevich,1983 Platynus cupreus (Dej.) Gibson and Treherne,1916 Pterostichus cupreus (L.) Adashkevich,1983 Pterostichus lucublandus (Say.) Gibson and Treherne,1916 Pterostichus melananus (H1.) Adashkevich,1983 Trechus obtusus (Erichson.) Hughes, 1959 Trechus quadristriatus (Schrink.) Hughes, 1959
Acarina.
Trombidium scabrum (L.) Gibson and Treherne,1916 - 296 -
Nematoda .
DD - 136. Welch and Briand,1960 Heterotylenchus sp. Nair and McEwen,1975
Fungi.
Conidioblus coronatus (Cohn.) Matanmi,Libby and Maxwell, 1974 Empusa muscae (Cohn.) Smith, 1927a. Entomophthora muscae (Cohn.) Strazdinya,1972 Entomophthora virulenta (Cohn.) Matanmi,Libby and Maxwell, 1974 Strongwellsea castrans (Batko and Weiser) Batko and Weiser,1965;Nair and McEwen,1975. - 297 -
APPENDIX 2
Synonyms of Trybliographa rapae (Westw.).
Kloet and Hincks' (1978) Check List of British Insects gives the following as being synonymous with Trybliographa rapae (Westw.):
Trybliographa britannica (Kieffer.) TrybZiographa crassicornis (Cameron.) Trybliographa erythrocera (Cameron.) Trybliographa fortinervis (Cameron.)
The following list of synonyms is from a more detailed survey made by
B. Bromand (pers.comm.) of the nomenclature and systematics of T.rapae.
It was in 1833 that Farmer (1835) found a cynipid and a fly pupa in a turnip field, and Westwood (1835) subsequently identified the insect as
Eucoila rapae (Westw.). The possibility of a connection between E.rapae and the fly pupa was, at that time, rejected. Thomson (1861) described
Eucoila octotoma (Thorns.) and stated as a synonym Cothonaspis scuteltaris
(Hart.). Kieffer and Dalla Torre (1910) noted Eucoila scutellaris (Cir.) and Trybliographa scutellaris (Forst.) as further synonyms of C.scutelLaris
(Hart.). As synonyms of Eucoela rapae (Westw.) Cameron (1890) states
C.scutellaris (Harr.) and Figites foveator (Dahlb.).
Slingerland (1894) recorded the hatching of numerous Trybliographa anthomyiae (Fletc.) from Delia radicum pupae and noted that the genus
Trybliographa was considered as a sub-section of the genus Eucoela in
Europe. Fletcher (1902) noted Eucoila anthomyiae (Ashm.) as a parisitoid of D.radicum. Washburn (1908) records Pseudoeucoila gillettei (Ashm.) as parasitising up to 46 percent of the pupae of cabbage root fly popula- tions. Schoene (1916) found Pseudoeucoila gillettei (Ashm.) to be very closely related, if not identical, to Cothonaspis rapae (Westw.). - 298 -
Treherne (1916) reported that Cothonaspis gillettei (Washb.) frequently
hatched from pupae of D.radicum. Gibson and Treherne (1916) found
Cothonaspis gillettei (Washb.) to be the same species as Fletcher (1902)
referred to as Eucoila anthomyiae (Ashm.).
Kieffer and Dalla Torre (1910) also mentioned Cothonaspis octotma
(Thorns.) and Cothonaspis rapae (Westw.), giving as synonyms, Eucoila
octotama (Thorns.), Trybliographa octotoma (Forst.) and Cothonaspis
octotoma (Kieft.), and Eucoila rapae (Westw.), Eucoeia (Trybliographa)
rapae (Cameron.), Cothonaspis rapae (Kieft.), Figites foveator (Dahlb.)
and Eucoila foveator (Dahlb.) respectively. These authors maintain that
C.rapae and C.octotoma were two independent species, but according to
Lundblad (1933) they are identical.
Meyer (1926)described Cothonaspis (Idiamorpha) gerasimovi (Meyer) as a
parasitoid of D.radicum, and Vasina (1927) recorded Eucoela (Psichacra)
spinosa (Hart.) as parasitising D.floralis and D.radicum. Bromand
(pers.comm.) is unable to conclude whether these cynipids were independent
species or are actually Trybliographa rapae. Muesebeck, Krombein and
Townes (1951) stated Trybliographa rapae (Westw.), with Eucoila rapae
(Westw.), and Pseudoeucoila gillettei (Washb.) as synonyms. Wishart (1957) noted that Cothonaspis ginettei (Washb.), Eucoila anthomyiae (Ashm.) and
Pseudoeucoila gillettei (Washb.) were the same species. Finally, Coaker
and Finch (1971) noted Idiomorpha rapae (Westw.) as a parasitoid of
considerable importance to D.radicum.
Synonomy of Trybliographa rapae (7 indicate uncertain synonyms):
Trybliographa rapae (Westwood)
syn: Idiomorpha rapae (Westwood) Cothonaspis rapae (Westwood) Cothonaspis rapae (Kieffer) Eucoela (Trybliographa) rapae (Westwood) Eucoila rapae (Westwood) - 299 -
Cothonaspis galettei (Washburn) Pseudoeucoila gillettei (Ashmead) Trybliographa anthomyiae (Fletcher) Eucoila anthomyiae (Ashmead) ? Eucoila octotoma (Thomson) ? Trybliographa Octotoma (Forster) ? Cothonaspis octotoma (Kieffer) ? Cothonaspis octotoma (Thomson) ? Cothonaspis scutenaris (Hartig) ? Eucoila scutellaris (Giraud) ? Yybliographa scutellaris (Forster) ? Eucoila foveator (Dahlbom) ? Figites fovea tor (Dahlbom) - 300 -
APPENDIX 3
Derivation of the no switch model using a special case of the Hassell, Lawton and Beddington (1977) model for a Type 3 Functional Response.
In parasitoids, the number of encounters with hosts during the total time of interaction, T, can be described by
N / P = a T e t s N (Al) where N is the number of encounters; Pt , the number of searching e parasitoids; a', the searching efficiency; Ts , the time available for search and Nt , the host density. The time available for search, T8 , is affected by time spent killing, eating, oviposition, cleaning, resting and other activities which are collectively known as handling time.
Thus, T = T - T N (A2) s h e where T is the handling time.
When two hosts are present, the time available for search, Ts , is further reduced and is thus given as,
T = T - T N - T N (A3) 8 hl el h2 e2 where T121 and Th2 are handling times of hosts 1 and 2, respectively and are the respective numbers of hosts encountered (Murdoch, Nel and Ne2 1973; Murdoch and Oaten, 1975). When Pt = 1, by substituting equation
(Aa) into (Al) we have,
N = a' N (T - T N re1 1 t1 hl el - TUNe2 ) (A4) N = a' N Or - T N ) • e2 2 t2 Th2Ne2 hl el
Searching efficiency, a', is defined by
a' = b N t (A5) where b is a constant describing the rate at which searching efficiency increases with host density. - 301 -
Substituting (A5) into (A4),
2 N = b N (r T N - TN ) el 1 tl h1 el e2 (A6) 2 N = b N (T - TN - T N ) e2 2 t2 e 2 hl el •
Rearranging, 2 2 b N = b N N (A7) 1 Ntl e2 2 t2 el
Substituting (A7) into (A6),
2 2 N = b N T - b N N T - b N N T (A8) el 1 t 1 t 1 e 1 hl 2 t2 e1 h2 •
Therefore,
12 b N T 1 t N (A9) el 2 2 (1 + b N T + b N T ) 1 t 1 hl 2 t2 h2
The number of hosts attacked by a parasitoid searching at random was
expressed by Thompson (1924) as
N = N [ 1 - exp (- N / N ) ] (A10) a t e t
Substituting (A9) into (A10),
- b NT 1 N = N [ 1 - exp ( ) ] CAM al tl 2 / + b N22' + b N T 1 hl 2 t2 h2
and similarly,
-b2Nt2T N = N [ 1 - exp ( ) .(Al2)] a2 t2 2 2 1 + b N T + b N T 1 tl hl 2 t2 h2 - 302 -
From equation (Al), when Pt = 1
N e
In this case, N e T s = 2 (A13) b N t
therefore from equation (A9),
T (A14)
- 303 -
APPENDIX 4
Experiment 4.1
Parasitoid density = 1
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 0 0 0
4 0 0 0 0 0
8 0 0 0 0 0
16 1 1 1 1 1
32 2 2 3 3 3
Experiment 4.2
Parasitoid density = 5
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 0 0 0
4 0 0 0 0 0
8 1 0 0 0 1
16 3 3 5 6 7
32 10 14 14 12 8
- 304 -
Experiment 11.2 (continued)
Parasitoid density = 10
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 0 0 0
4 0 0 1 0 0
8 1 2 1 0 1
16 4 4 5 4 6
32 14 12 12 13 16
Parasitoid density = 15
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 0 0 0
4 0 0 0 0 0
8 1 1 1 3 0
16 5 5 4 4 10
32 12 11 12 10 16
- 305 -
Experiment 4.2 (continued)
Parasitoid density = 20
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 0 0 0 4 1 0 0 0 1
8 1 2 1 0 2 16 3 5 5 6 4 32 8 12 15 16 8
Experiment 4.3
Parsitoid density = 1
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
12 0 0 0 2 0
12 0 1 1 0 0
12 0 0 2 0 1
12 0 1 0 1 0
12 2 0 0 0 0 - 306 -
Experiment 4.3 (continued)
Parasitoid density = 5
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
12 0 1 2 0 1
12 2 0 4 0 0
12 2 0 2 3 1
12 0 1 4 0 3
12 2 1 0 0 6
Parasitoid density = 10
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
12 2 2 1 0 1
12 0 3 0 5 1
12 4 0 0 4 0
12 2 0 2 0 3
12 0 1 2 0 4 - 307 -
Experiment 4.3 (continued)
Parasitoid density = 15
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
12 1 3 5 1 1
12 4 3 1 3 0
12 2 2 4 1 2
12 2 3 3 1 1
12 2 4 3 2 1
Parasitoid density = 20
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
12 3 3 3 3 2
12 3 1 4 3 4
12 0 0 6 4 5
12 3 4 1 4 3
12 2 3 3 1 4
- 308 -
Experiment 5.1
Parasitoid density = 5
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5 6 7 8 9 10
2 0 0 0 0 0 0 0 0 0 0'
4 0 0 0 0 0 0 0 0 0 0
8 0 1 1 0 1 00 1 0 0
16 2 3 3 3 3 1 3 3 3 3
32 10 10 10 10 9 11 11 9 11 10
Parasitoid density = 10
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5 6 7 8
2 0 0 0 0 0 0 0 0
4 0 1 1 0 0 0 0 0
8 2 3 3 2 1 2 2 1
16 7 6 6 9 8 6 7 5
32 16 19 18 15 13 15 16 16
- 309 -
Experiment 5.1 (continued)
Parasitoid density = 15
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 0 1 0 1
4 1 1 2 0 1
8 3 3 5 2 5
16 7 7 8 8 12
32 19 20 17 15 21
Parasitoid density = 20
Number of hosts Number of hosts parasitised in patch Replicate 1 2 3 4 5
2 0 1 0 1 1
4 0 2 1 1 2
8 1 3 3 4 5
16 6 10 9 7 9
32 23 19 17 15 21 - 310 -
Experiment 5.2
1983
Replicate 1 2 3 4 5 6 7 8 9 10
Initial number = 64
Number collected 26 29 27 28 33 30 29 35 35 Number parasitised 13 14 10 11 18 10 17 23 11
Initial number = 32
Number collected 23 18 21 17 27 25 21 27 26 Number parasitised 9 7 6 7 5 8 6 6 10
Initial number = 16
Number collected 16 15 8 14 14 16 15 15 16 14 Number parasitised 4 3 5 4 3 3 4 2 3 4
Initial number = 8
Number collected 8 8 5 8 7 6 8 8 8 8 Number parasitised 0 0 2 0 1 0 2 1 1 1
Initial number = 4
Number collected 4 4 4 4 4 4 4 4 4 4 Number parasitised 1 0 0 0 1 0 0 0 0 0
Initial number = 2
Number collected 2 Number parasitised 2 -311 -
Experiment 5.2 (continued)
1984
Replicate 1 2 3 4 5 6 7 8 9 10
Initial number = 64
Number collected 22 26 32 20 23 28 40 27 32 31 Number parasitised 12 14 15 10 11 13 23 13 15 16
Initial number = 32
Number collected 25 23 19 21 18 20 26 27 16 19 Number parasitised 13 12 9 11 7 9 11 10 6 5
Initial number = 16
Number collected 11 10 12 7 11 9 10 8 11 11 Number parasitised 5 4 4 4 3 3 2 1 3 4
Initial number = 8
Number collected 4 5 5 8 6 7 7 8 8 6 Number parasitised 1 1 0 2 0 2 2 1 2 0
Initial number = 4
Number collected 4 3 4 4 4 4 3 4 4 3 Number parasitised 0 0 0 0 0 0 0 1 0 0 - 312 -
Experiment 5.3
1981 1982A 1982B 1983 1984 1 1 NPNPNP NPINP N P'NP
10 1 8 4 8 4 30 5 1 00 00
2 0 4 0 12 6 92 40 20 26 15 ..
7 3 19 8 6 2 3 1 4 0 0 0 2 0
2 0 8 1 2 0 70 30 1 0 94
5 1 2 0 5 1 00 20 7 1 1 0
10 3 9 1 6 2 11 3 00 30 00
12 5 5 1 9 5 20 50 103 5 1
4 0 1 0 10 5 1 0 20 00 6 2
10 1 5 0 2 0 30 20 70 23 13
4 0 20 5 5 2 1 0 00 208 00
3 0 9 1 4 1 18 8 0 0 2 0 1 0
8 1 1 0 8 3 20 4 0 11 5 12 2
7 1 3 1 16 6 2 0 2 0 0 0 3 1
5 1 14 3 3 0 249 00 103 00
1 0 3 0 2 0 15 6 0 0 9 2 3 1
7 1 8 2 3 0 90 12 3 1 0 4 0
5 1 13 3 12 4 20 8 0 0 17 8 31 18
2 0 4 0 4 1 30 20 6 2 00
5 0 7 4 28 23 1 0 208 7 1 148
4 1 0 0 30 21 20 9 1 0 22 12 13 7
2 0
3 0
Key: N : Number of pupae collected (per sample)
P : Number of pupae parasitised by T.rapae - 313 -
Experiment 6.1
Egg mortality
Initial number Number of eggs collected of eggs Replicate 1 2 3 4 5 6 7 8 9 10
2 2 1 1 2 2 2 2 1 2 2
4 3 4 2 3 4 4 3 3 2 4
8 7 7 6 5 7 7 7 6 4 6
16 12 10 11 14 15 16 13 12 8 9
32 26 25 23 24 18 15 20 22 22 16
64 43 44 52 48 36 42 49 56 60 43
128 96 84 111 72 64 53 116 103 112 93
256 98 170 143 132 106 116 109 93 154 164 - 314 -
Experiment 6.1 (continued)
Pupal mortality 1 9 8 3
Replicate 1 2 3 4 5 6 7 8 9 10
Initial number = 32
Number collected 27 29 25 16 30 27 30 32 14 32 Number parasitised 1 0 0 0 0 0 2 0 0 0
Initial number = 16
Number collected 14 10 13 11 14 13 11 16 14 16 Number parasitised 0 0 0 0 0 0 0 0 0 1
Initial number = 8
Number collected 8 8 8 6 8 8 4 7 8 8 Number parasitised 0 0 0 0 0 2 0 0 0 0
Initial number = 4
Number collected 4 4 2 3 3 2 2 4 4 4 Number parasitised 0 0 0 0 0 0 0 0 2 0
Initial number = 2
Number collected 2 2 0 2 2 1 2 2 2 2 Number parasitised 0 0 0 0 0 0 0 0 0 0 - 315 -
Experiment 6.1 (continued)
1984
Replicate 1 2 3 4 5 6 7 8 9 10
Initial number = 32
Number collected 24 26 20 25 24 24 28 23 22 21 Number parasitised 1 2 1 0 1 1 3 0 2 1
Initial number = 16
Number collected 12 15 14 10 15 13 9 12 11 12 Number parasitised 1 3 3 1 2 2 2 4 1 2
Initial number = 8
Number collected 6 6 8 7 6 5 5 4 7 6 Number parasitised 1 1 3 2 0 1 0 1 2 2
Initial number = 4
Number collected 3 2 3 2 3 3 4 2 4 Number parasitised 0 0 1 0 1 1 1 2 0
Initial number = 2
Number collected 2 2 2 1 2 2 1 1 2 2 Number parasitised 1 0 1 0 1 0 1 1 2 2 - 316 -
Experiment 6.1 (continued)
Data for 'k-value' analysis
Key: N - Initial number of eggs
N - Number of pupae collected
P - Number of pupae parasitised by T.rapae
F:41 - Number of pupae parasitised by A.baineata E - Number of pupae failing to eclose
1983
N N PA E N N T P C PT C P A E
4 2 0 1 0 32 10 4 2 0 4 3 1 1 0 32 9 3 0 0 4 2 1 00 32 16 7 1 1 4 2 0 20 32 5 0 1 0 4 3 0 1 0 32 8 2 1 1 4 3 0 00 32 10 3 1 0 4 2 1 00 32 12 4 3 2 4 3 2 0 1 32 4 0 1 0 4 3 0 1 1 32 16 6 4 0 4 3 0 20 32 9 1 1 1 4 2 0 1 0 32 12 4 1 0 32 6 1 1 0 8 2 0 00 8 6 2 20 64 16 5 6 0 8 2 0 00 64 16 8 1 1 8 4 1 02 64 11 4 3 1 8 2 0 1 0 64 12 4 3 0 8 2 0 00 64 10 3 2 0 8 2 0 00 64 9 3 2 0 8 6 1 20 64 10 3 2 0 8 2 1 00 64 14 5 5 1 8 2 0 1 1 64 10 3 4 2 8 4 1 2 1 64 16 6 3 0 8 4 0 20 64 12 4 3 2 8 4 0 1 1 64 10 3 1 2 64 8 2 4 0 16 7 2 1 0 64 10 2 0 3 16 8 3 2 1 64 10 2 4 0 16 3 0 0 0 64 15 4 2 1 16 4 1 1 0 64 16 5 4 0 16 9 2 2 1 16 3 0 0 0 128 9 2 1 1 16 9 3 2 0 128 10 3 1 1 16 10 2 3 1 128 8 2 1 0 16 2 0 0 0 128 1 0 0 1 16 10 3 2 0 128 5 1 0 0 16 2 0 0 0 128 3 0 0 0 16 10 4 2 0 128 10 3 1 1 16 2 0 0 0 128 6 1 1 1 128 13 4 2 0 32 14 5 1 1 128 10 4 0 1 32 8 2 2 0 128 6 1 0 1 32 3 0 1 0 128 5 1 0 0 32 2 0 1 0 128 10 5 1 0 32 8 0 2 1 128 4 1 1 0 - 317 -
Experiment 6.1 (continued)
1984
N PT P E N N PT PA E Na A C
4 2 0 1 0 32 10 1 4 0 4 2 0 1 0 32 10 0 6 0 4 2 0 00 32 11 1 0 1 4 2 0 1 0 32 12 2 0 0 4 2 0 1 0 32 12 3 3 0 4 2 0 1 0 32 11 0 7 0 4 2 0 1 0 32 10 0 7 1 4 1 0 00 32 11 1 6 0 4 2 0 1 0 32 10 1 0 0 4 2 0 00 32 11 0 3 0
8 5 1 1 0 64 20 3 1 0 8 3 0 1 1 64 15 1 0 1 8 2 0 00 64 18 2 1 0 • 8 3 0 1 0 64 19 2 8 0 8 4 0 1 0 64 15 1 0 0 8 2 0 1 0 64 20 4 4 1 8 3 1 1 0 64 14 0 2 2 8 5 0 1 1 64 11 0 0 2 8 4 0 1 0 64 22 4 0 1 8 4 0 1 0 64 19 1 1 1
16 6 1 0 1 128 28 8 2 0 16 6 0 1 0 128 26 6 4 0 16 5 0 1 0 128 28 6 2 2 16 7 1 1 0 128 31 13 2 0 16 8 2 1 0 128 29 7 10 0 16 5 0 1 0 128 24 6 4 1 16 8 1 1 0 128 27 8 6 0 16 8 1 1 0 128 22 6 0 1 16 7 0 1 1 128 35 9 2 3 16 7 0 1 0 128 28 8 0 0