1 General Introduction

If the karate-ka (student) shall walk the true path, first he will cast aside all preference. Tatsuo Shimabuku, Grand Master of Isshin-ryu Karate

1.1 The Importance of Insects ~30% of the plants we grow for food and materials. Because of their great numbers and diversity, insects Insects transmit some of these pathogens. While have a considerable impact on human life and indus- weeds can often reduce pest attack, they can also try, particularly away from cities and in the tropics. harbour the pest’s enemies or provide alternative On the positive side they form a large and irreplace- resources for the pest itself. Then in storage, insects, able part of the ecosystem, especially as pollinators mites, rodents and fungi cause a further 30% loss. of fruit and vegetable crops and, of course, many Apart from such biotic damage, severe physical con- wild plants (Section 8.2.1). They also have a place ditions such as drought, storms and flooding cause in soil formation (Section 8.2.4) and are being used additional losses. For example, under ideal field increasingly in ‘greener’ methods of pest control. conditions new wheat varieties (e.g. Agnote and Biological control using insects as predators and Humber) would give yields of ~16 tonnes/ha, but parasites of pest insects has been developed in the produce typically about half this under good hus- West for over a century, and much longer in China. bandry. Pre-harvest destruction due only to insects More recently integrated pest management (IPM) is 10–13% (Pimentel et al., 1984; Thacker, 2002). and conservation biological control (CBC) are being Losses are probably higher in the Developing deployed to better effect. World. Hill (1997) and Boyer et al. (2012) estimate Entomology has played a major role in the devel- 30–40% of total crop losses globally. Polis (1999) opment of ecology and other branches of biology states ‘Worldwide, ... insects take about as much crop such as genetics, physiology and behaviour. This is production as is used by humans’, although other not only because insects form the major part of the data (Reynolds, 2012a) suggest that this estimate is terrestrial fauna, but also because they offer a con- too high. But without crop protection, chemicals venient method of study. Their relatively small size included, losses could be 30% higher than they are leads to easy handling and their abundance facilitates with it (Oerke, 2006). Over the years there has been sampling and, in turn, a numerical analysis of the a shift of expenditure – insects now cost us large results. Their main disadvantage is that there are too amounts for crop protection, hopefully to lessen many of them. So many orders, families and species their effect. The annual bill for agricultural insecti- exist that learning about their immense diversity cides is now approximately US$7 billion in North takes a long time and not inconsiderable effort. America, and more than US$20 billion worldwide. Also, many people are entomophobic: they just do Even so, their effectiveness is variable. Naturally, not like insects and proceed in ignorance to belittle these estimates are but a fraction of the total because their far-reaching effects on people and the envir- the costs of application and wasted time should onment. After you read this book you will not be also be put on the account. among them. This situation has promoted a huge research But of course, some insects have a negative side, effort, but since agriculture in its widest sense is the and in a few this side is considerable. Before harvest world’s biggest productive industry, and since research they, together with weeds and pathogens, destroy scientists are, in the main, dedicated people working

© CAB International, 2020. Ecological and Economic Entomology: A Global Synthesis (ed. B. Freeman) 1 for low salaries, generally this has been cost effective. agriculture. There are direct and indirect effects. A Premiership footballer gets twice as much in a Both farmers and livestock may suffer insect bites, week as the average scientist gets in a year. Hopefully, become victims to their juvenile stages or get future generations will wonder at this past stupid- infected with insect-borne diseases such as malaria ity. One of the reasons why improving pest control and dengue. As we will see, only a few insect species is critical, is that although new crop varieties have are pests; most are beneficial. The number of import- greatly increased production (Oerke, 2006), trad- ant pests is around 0.1% of the vast number of itional crops had more innate resistance to insect described insect species (about 1000–2000 species damage. Traditional rice in Asia had losses of only a in total). With time, some species gain and others few per cent, while modern varieties can have losses recede in their importance. This is because new crops around 25%. Even so, they produce five times as are developed and grown and new forms of hus- much grain per hectare and that is the bottom line; bandry are devised, but also because agro-chemicals a basic principle. are misused. Insects also migrate and/or change The widespread use of insecticides, fungicides and under climatic and evolutionary influences, while weed killers has brought environmental pollution management is rarely fully informed. in its train. Conversely, in traditional African agri- culture little is spent on chemicals, but losses from 1.2 Insect Size pests are very apparent. Environmental degrad- ation in Africa is due largely to deforestation; in In the scale of life, insects are of small to medium Europe that has happened already. Only if we can size. Mymarid wasps that parasitize insect eggs learn to manipulate our environment and agro- weigh <1 mg, while at the other end of the scale ecosystems in particular in permanent ways, with Goliath beetles may attain 40 g, a range >40,000 mg. low recurrent expenditure, would we have defeated Hamilton (1996, p. 386) provides an even greater enemy insects. This has been achieved in a few range: Titanus giganteus from palm logs in Brazil cases. But ‘permanent’ is euphemistic when applied to are a million times bigger than ptilinid beetles biological systems: the playing field is uneven and (Ptinella). Their size relative to other terrestrial the rules partly known. While limits exist (Arnold, animals, their size within the range for insects and 1992), evolution works constantly (Haldane, 1954; even their own species have basic consequences for Trivers, 1985), adjusting the positions of all the their physiology and ecology (Price, P.W., 1997). living players. We hear fables of fleas scaled to the weight of a Progress in our favour has continued for several man jumping over famous public buildings. This decades, but an idyllic final solution is still far off. nonsense is the result of a naïve linear scaling of Old organic insecticides such as DDT were applied at both weight and power. But weight is a cubic func- an average rate of 1 kg/ha; now alpha-cypermethrin tion of body length, whereas muscular power is is applied at around 10 g/ha. These developments only a squared function. Doubling in weight pro- come not only within the ambits of organic chem- duces much less than doubling in power. Small size istry, ecology, largely applied ecological entomology also allows insects to exploit the great physical and population dynamics (Berryman, 1991b), but variation in their environments (Section 10.1.1). also those of economics and management. And any Another critical effect is that the smaller the organ- system used to combat insects must dovetail into the ism, the greater its surface area (a squared func- control of other pests, agricultural practice in gen- tion) relative to its weight. Big animals are in the eral and into economics. The nearest to the ideal grip of gravity, little ones are more affected by sur- solution we have come are biological control and face effects. Small insects trapped in a film of water IPM, but these methods do not always work and there may be unable to free themselves. These relationships may still be an environmental backlash (Pimentel give us a glimpse into the foreign physical environ- et al., 1984). Related techniques of landscape man- ment of the insect, for example, how a fly can land agement and CBC are still being developed. But upside down on a ceiling. ignorance, lack of aesthetic awareness and avarice The world is relatively a much larger place for a continue to be important social factors. small animal than it is for a large one (Hutchinson, Insects attack not only our field, forest and orchard 1959; Morse et al., 1985). To continue with insect crops, but also our domesticated animals and our- size discussion, our mymarid wasp develops within selves, making it more difficult for us to practise the minute confines of a moth’s egg, but the larva

2 Chapter 1 of the big moth Manduca sexta may have to eat an and Denno, 1997; Marden, 2000). Insect size affects entire tomato plant for development. Many phyt- both mobility and reproduction. Insect flight muscle ophagous insects live inside their plant food (endo- is of two types: the synchronous or neurogenic type phytic). Some cereal beetles can live out their juvenile in which each neural stimulus produces a single lives within single grains. Indeed, the rather low contraction; and the asynchronous or myogenic metabolic rate of larval forms allows them to sur- type in which it produces multiple contractions. vive in cryptic places. Here oxygen is deficient, but Unsurprisingly, wing-beat frequency, wing loading, they avoid desiccation and predation. Several moth mass-specific power output and fuel consumption caterpillars, like the teak defoliator (Section are usually greater in the latter. While insect flight 5.2.1.4(k)), roll up leaves and hide therein, and sev- mechanisms have similarities to those of birds, their eral species pupate in them or use a small chink in wings have no intrinsic muscles so changes in wing the bark of a tree. The small size of insects in gen- shape are controlled by structural mechanisms. Indeed, eral means that their environment, and especially controlled deformability is the essence of insect wing their hygrothermal environment, is very patchy. design and function; they are elegantly adapted flex- Again because of the physics of scaling, flight is an ible aerofoils (Wootton, 1992). efficient mode of locomotion for insects (Ellington, Insect shape is another consideration, especially in 1991; Harrison and Roberts, 2000); we need think relation to hygrothermal control. Compact insects only of the prodigious distances covered by migrating like higher Diptera and many beetles have less body butterflies like Vanessa cardui (Section 12.3.3.2). surface for a given mass than elongate ones, such as While the rate of energy consumption in flight is dragonflies, locusts and crane flies. The latter poten- much greater than that of crawling, the total ener- tially desiccate more easily and some are more getic cost/km is far less (Kammer and Heinrich, 1978). affected in flight by wind (Freeman and Adams, This is partly due to the physics of flight, but also 1972). But elongate insects like grasshoppers and includes wind assistance and avoidance of obstruc- asilid flies are better at using differential orientation tions on the ground. This is critical for small insects to gain or lose heat as the situation demands (May, due to the effect of size on the fractal nature of 1979; Morgan and Shelly, 1988; see also Section their world, they can take only small steps on the 10.1.1). When too cool they orientate to cast a big ground (Section 12.2.6). The evolution of mobility shadow, or when too hot cast a small one, or even in most adult insects alters their spatial ecology take a position in the shade of a grass stem. In some relative to that of their juveniles and to all other Orthoptera such as Schistocerca and Orphulella, terrestrial invertebrates (Section 12.3.4.4(c)). It allows the thorax is flattened ventrally and can be pressed them to migrate, seek resources and control landing, down on warm ground, therefore gaining free heat. and so are able to exploit fully the three-dimensional The high metabolic rate of most adult insects nature of their habitat (Roff, 1990; Marden, 2000), contrasts them with nearly all other terrestrial inver- attributes extending back more than 350 million tebrates, and is a consequence of their efficient years ago (Ma). Flight has continued to evolve over system of gaseous exchange: oxygen in and carbon this immense period, allowing longer migration and dioxide out. Their unique tracheal system of fine increasingly sophisticated resource seeking (Section air tubes, assisted in active insects by ventilated air 10.2.4.1). Vagrant insects may migrate >500 km in sacs, permits rapid gaseous exchange (Price, P.W., a single generation. The inception of flight brought 1997; Dudley, 2000; Harrison and Roberts, 2000). about a refinement in risk/reward dynamics (q.v.; Even simple diffusion of oxygen down tracheae is means which see, refer to Glossary throughout text) very much faster than it would be through tissue. and mitigates the changing heterogeneity of the Compared to vertebrate blood systems, tracheal environment. While parasitic worms produce huge systems are light, promoting a higher power : mass numbers of eggs and larvae that seek new hosts, ratio. Muscular vibration also assists respiratory these are earth bound. Aphids and fruit flies fly exchange, and differences in pressure between the aloft, greatly extending their area of environmental front and back of some flying insects, the Bernoulli scanning. entrainment, can pull gases through them. Insect But to fly an insect requires >12% of its body mass metabolism is unconstrained by a lack of oxygen if in flight muscle. Since muscle is metabolically expen- they have access to air. Indeed the flight muscle of sive to build and maintain, there is often a trade-off euglossine bees (Section 8.3.6) is the most active between flight and reproductive capability (Zera tissue known (Casey et al., 1985; Dudley, 1995).

General Introduction 3 All flight muscles are liberally supplied with mito- as the group to which they belong, and to know the chondria (Marden, 2000), but inactive insects essentials of their biology. After that, one must use consume little oxygen, while during inclement sea- appropriate taxonomic keys. An applied entomolo- sons, insects frequently enter a hormonally mediated gist would be worse than incompetent if he/she state of low metabolic activity and morphogenesis could not separate, for example, a predatory cara- (Tauber and Tauber, 1981) called diapause (Section bid beetle from a wood-feeding tenebrionid beetle 10.2.3). or a leaf-eating chrysomelid beetle. Misidentification can lead to inappropriate action, which is generally worse than no action at all. But the level to which 1.3 Insect Taxonomy in Relation identification should go varies – it may be adequate to Physiology and Ecology to recognize a family in some circumstances, but on While physiology and ecology relate to insect size, others one must identify the genus or the species. they also relate to insect classification, but of course Now, as we noted, there are an awful lot of insect for entirely different reasons. First, the basic split species. Over a million have been described. They into exopterygotes and endopterygotes (Section are arranged in ~30 orders and ~1000 families, each 1.4) has important ecological consequences. The with its own special morphological and often eco- lack of a pupa in the former group means that there logical characteristics. When all insect species are is, for terrestrial species at least, no fundamental described, and we have a long way to go, there will change in lifestyle between the juvenile and the be several million of them, maybe more (Hammond, adult. The degree of transformation of a squirming 1992; Dudley, 2000; Reynolds, 2011). But while maggot in a carcass to a fast-flying adult blow fly Hutchinson (1953) mused on the great abun- would be impossible in an exopterygote, although dance of species, Felsenstein (1981) inquired, given in the palaeopteroid orders (Section 1.4) changes the dynamics of speciation (Section 9.10), why between an aquatic nymph and a flying adult are there are not even more. very marked. Therefore in the Odonata, nymphs Although this book is not general entomology, in are modified as aquatic predators and adults as order to get the most out of it some familiarity with aerial ones. Again, most endopterygotes suffer from insect classification and biology is essential. We will having two, non-feeding immobile stages (i.e. egg refer to many insect species by scientific name: and pupa) that possess only passive or physiological many plant pests, vectors of disease, predators and defences (Danks, 2007). Behavioural defences that parasitoids, for example. They are named as a ref- depend on movement are debarred (Section 10.1). erence and to give beginning students a glimpse at Second, insects in certain groups are specialized their enormous diversity. You do not have to learn towards particular lifestyles. Herbivory is found them all! (Forthwith I will usually lapse the term mainly in the six largest orders (Section 2.3.1), sug- ‘beginning students’ to just ‘students’, still implying gesting that the habit itself has promoted speciation the possibly fortunate young, but also recognizing (Section 9.10). Numerous Heteroptera are terres- that we are all still learning.) I provide here some trial or aquatic predators. The Lepidoptera are guidelines as to how familiarity with insect classifi- mainly herbivorous. Female Hymenoptera, apart cation may be achieved without undue pain, a from phytophagous sawflies, are largely predators familiarity that does not breed contempt. These and parasitoids (Schoenly, 1990), which is regarded guidelines should be used in conjunction with some as a consequence of their evolving a sting. But comprehensive textbooks. many Diptera and Coleoptera are similarly aggres- There are two traditional textbooks in English. sive towards other insects. Lifestyle, to an extent, is Imms’ General Textbook of Entomology, revised linked to taxonomy. by O.W. Richards and R.G. Davies in 1988, is an imposing two volumes (we quote books by the names of their authors, not by their titles). This work is bet- 1.4 Learning Insect Classification ter for the European and Old World insect fauna. Because insects are so numerous and so diverse, a Then there is Borror and DeLong, which has been competent economic entomologist must be, at the revised by C.A. Triplehorn and N.F. Johnson succes- outset, a competent general entomologist. For sively (Triplehorn and Johnson, 2005). This work is the beginner this is a daunting prospect. It means directed towards North American insects and is replete being able to recognize living insects on sight as far with excellent illustrations, combining simplicity with

4 Chapter 1 accuracy. Both books, however, are completely com- which arose somewhat later (Scott et al., 1992). prehensive. The classifications they use are sub- Next, it is cardinally important to remember that stantially the same, although they differ in some the Pterygota come in two quite different sorts, a particulars. While Richards and Davies’ revision is difference that is based on the type of development a bit dated it is more detailed. Owain Richards was from egg to adult. a man of encyclopaedic knowledge of insects and Like all arthropods, insects have a dead external ecology. He once told me in a rare moment of levity skeleton (exoskeleton) functioning for support and that since retirement he no longer worked 18 hours protection. It comprises diverse proteins, contains a day. ‘Only twelve’, his wife added. He used his chitin fibrils and is surmounted by a protective time efficiently, never greeting you normally, and epicuticle. Complex structural interplay between with no preface of pleasantries he would continue the protein and chitin components gives the cuticle straight into the previous scientific conversation diverse properties of physical protection and flexi- that you had been having, adding new information bility, as in other composite materials such as fibre- and perspective. Quite an intellectual ordeal when glass. But since the exoskeleton is dead it has to be I was young. Also worth delving into is J.H. shed periodically, permitting the insect to grow and Comstock’s (1940) An Introduction to Entomology, develop, like a young medieval prince having to be which went into at least nine editions, and bears fitted annually with a new suit of armour as he the author’s austere portrait at the front. grows into a man. Insect growth is cast into a series Recently, Gillott’s (2005) comprehensive text has of stages, or instars, between sheddings. Apart from gone into its third edition. Then there are Arnett’s elaborate organs such as antennae, and compound (1985) handbook of American insects, Chapman’s eyes that can see everywhere at once, insects perceive (1998) textbook on the general structure and physi- the external world with a complex array of sensory ology of insects, Daly et al.’s (1998) work, which hairs passing through this armour; as Taylor and contains a section on systematics and biology, and Krapp (2008) put it: they ‘bristle with sensors’. Grimaldi and Engel (2005). There is also an insect In some insects the wings develop gradually on encyclopaedia edited by Resh and Cardé (2003). the outside as four increasingly visible buds as the Several books exist that cover only a single insect individual passes from instar to instar. They are order, such as Dolling (1991) on the Hemiptera, hence called Exopterygota (‘outside-winged ones’) Gauld and Bolton (1991), Austin and Dowton (2000) or Hemimetabola. They have been on Earth since on the Hymenoptera, Ford (1955) on moths and the Upper Carboniferous over 300 Ma, although Oldroyd (1964) on Diptera. several orders, such as the Palaeodictyoptera, have When I was taught entomology at university we become extinct (Labandeira and Sepkoski, 1993). started at Order 1, the Thysanura, and ended up at In the Exopterygota, we shall call the stage that comes Order 29, the Strepsiptera. This was the wrong way out of the egg a nymph. It usually looks something to do it. It was rather like a temporal version of like a miniature, wingless adult and as it moults Columbus’ first voyage to the Americas. It is said successively it gets to look more and more like a that when he went he did not know where he was wingless adult. In the final moult the wing-buds going; when he arrived he did not know where he expand so forming two pairs of wings and it is an was; when he got back he did not know where he adult. It does not moult any more. had been; and he did it all on public money. So that Then there is the other, much larger group in this does not happen to beginning students I pro- which the wings develop on the inside of the juvenile vide the scheme which now follows. stages, so that they are at first invisible externally. The scheme consists essentially of looking at They are, hence, called the Endopterygota (‘inside- insect classification in plan; you see all the essen- winged ones’) or Holometabola. Endopterygote tials together. One learns the most important things orders are more recent, arising about 260 Ma in first, the lesser things subsequently and, like a Google the Permian, and more recently have expanded in map, zoom in progressively on layers of increasing numbers in concert with the increasing diversity of detail. But before starting we put the primitively flowering plants, although this is not the only factor wingless insects, the sub-class Apterygota dating in their success (Labandeira and Sepkoski, 1993). from the Lower Devonian Rhynie chert some 400 Ma, The creature hatching from the egg (eclosion) looks to one side. We are left with the vast majority of nothing like an adult and each time it moults it does insects, the sub-class Pterygota, or ‘winged ones’, not get to look any more like an adult, just bigger.

General Introduction 5 It is a larva, a specialized feeding stage. A stage of enemies are different in each phase, adding com- change, the normally sedentary pupa, has evolved plexity to their dynamics (Lewis, 1997). allowing this stage to change into an adult. The adult, which emerges from the pupa, is the stage 1.4.1 Adult insects modified for dispersal and reproduction, usually in that order. It does not moult any more either. Within this great sub-class Pterygota there are only Insect stages differ in mobility. These differences, seven groups that one must learn in order to navi- while simple, are fundamental to their ecology. All gate insect classification. These are placed in what eggs and endopterygote pupae are sedentary (unu- I call the ‘four-square diagram’ (Fig. 1.1). Vertically, sual pupae will be noted later). All nymphs and lar- the diagram divides the Pterygota according to vae can move to a variable extent, although a few, whether they are exopterygotes or endopterygotes. like maggots and many boring beetle larvae, lack Horizontally, it divides them according to the type legs. Most adult insects have wings and can fly, of adult mouthparts. These are either the more primi- although a few, like ectoparasitic fleas and lice, do tive, biting or mandibulate sort, or the more advanced, not and therefore cannot. Here the term ‘immobile sucking sort that evolved from them (q.v.). This stages’ refers to eggs and pupae, while ‘mobile stages’ horizontal split according to mouthparts is useful are the rest, although adult scale insects become because it gives an entomologist a clue as to what anchored to their plant food. Thus, the ecology and type of insect did the observed damage to a crop population dynamics of insects change successively plant, when, as is often the case, the culprit is no as they develop from egg to adult. Following this, the longer around to be identified. Sucking insects dynamics of endopterygotes are often more com- often transmit pathogenic micro-organisms (I will plex than are those of exopterygotes as there are four, often use the shorter term ‘microbes’), both of ani- not three, different life stages. Also, larvae are more mals and plants. Biters variously chew bits out of different anatomically from adults than are nymphs the plant, damaging the cells and releasing elicitor from adults, and generally live in different microen- compounds (Section 2.4.2), but rarely transmit vironments. The exopterygote orders Odonata and plant pathogens. When a leaf is damaged, the bits Thysanoptera (thrips) are particular exceptions. The removed relate to the size and behaviour of the former (Section 1.3) comprises aquatic predators biter, producing diagnostic patterns. Those of two as juveniles and aerial predators as adults, and teak defoliators, Hyblaea and Eutectona, are quite hence occupy very different media. Thrips usually different (Nair, 2007). Suckers also have a vari- start life as concealed eggs, feed on plants as active ety of feeding mechanisms (Mitchell, 2004). nymphs and then become quiescent in the soil before The Heteroptera (larger) often damage tissue while the dispersive adult develops. In both cases their feeding, leaving diagnostic spots, blemishes and

BITING SUCKING Palaeopteroids Hemipteroids EXOPTERYGOTA Orthopteroids (Heteroptera, Auchenorrhyncha, Sternorrhyncha) Hymenoptera Lepidoptera ENDOPTERYGOTA Coleoptera Diptera

Fig. 1.1. The four-square diagram. This is all one needs to learn about insect classification at first. Once it is off pat you have a map of the insect world, continent by continent, so to speak. As you learn about other insect groups, the smaller orders, sub-orders and large families, you place them in this framework. For example, the order Trichoptera (caddisflies) belongs at the vertical division of the endopterygotes. These insects are a bit like moths (sucking mouthparts) but have biting mouthparts. This is like putting countries into the continents. The Hemiptera were formerly divided into the Heteroptera and Homoptera, but the latter is now split into the Auchenorrhyncha and the Sternorrhyncha, which are each given sub-ordinal status. The former bugs are distinguished by having a terminal arista to the antenna, lacking in the latter. In the Sternorrhyncha the base of the rostrum arises between the fore coxae. In future, I refer to these groups jointly as homopteroids.

6 Chapter 1 deformations at the site. They may lacerate cells larvae have biting mouthparts, although some are (Lygaeidae), use pectinase to macerate them (Miridae) much modified. Larval Diptera Cyclorrhapha gen- or employ salivary sucrase to induce osmotic unload- erally have rasping mouthparts, but adults have ing from the phloem (Coreidae) (Miles and Taylor, imbibing or piercing and sucking ones. Lepidopteran 1994). Many (smaller) homopteroids insinuate their caterpillars have chewing mouthparts, but the mouthparts between the cells to seek vascular tissue adults usually suck nectar through a coiled probos- (Howe and Jander, 2008). Sheath saliva is secreted cis. These stages have different feeding strategies along the stylet’s path, and watery saliva at the feed- and occupy different trophic levels. Biting stable ing site contains a complex of enzymes (Kaloshian, flies are detritivores as larvae and micropredators 2004). While these bugs leave less obvious damage, the as adults (Section 7.1.1.2). One species occupies plant’s tissue may deform and/or become chlorotic. two trophic levels (Murdoch, 1966b). But we They also transmit most plant viruses (380 species, must grapple with the major types of endoptery- 27 genera). The type of mouthpart also relates to gote larvae. Luckily, there are only a few characters other aspects of the insect’s biology, which we will (Fig. 1.2). note in due course. Caterpillars of the Lepidoptera usually have Recapping, the major phases in insect evolution several ocelli (simple eyes), three pairs of thoracic are as follows (the arrows indicating increasing legs, four pairs of abdominal legs and a pair of levels of sophistication): terminal claspers. They have a complete head cap- sule with vertical jaws and a full set of spiracles. Apterygota (Devonian) → Exopterygota (Carboniferous) The main exceptions are caterpillars of the geome- → Neoptera (Upper Carboniferous) → trid moths, which have a single pair of abdominal Endopterygota (Permian) legs, and those of some blue butterflies (Lycaenidae) associated with ants, in which the legs are rudi- mentary. Sawfly caterpillars (Hymenoptera) are 1.4.2 Eggs and juvenile insects amazingly similar except for having only a single Insect eggs are produced in paired ovaries within pair of ocelli, more than four pairs of abdominal the abdomen. Each ovary consists of several tubu- legs (Section 5.2.1.3(b)) and often an oily appear- lar ovarioles in which eggs are produced in a linear ance. Beetle larvae are rather like caterpillars too, chain. Highly fecund insects have many more ovari- but they have no abdominal legs. The larvae of oles than do those with low fecundity, while larger buprestid, cerambycid and curculionid beetles conspecific females usually have more ovarioles than have no legs at all. This relates to their boring habit. smaller ones. Panoistic ovaries lack nutritive cells, Leglessness, in this instance, is a general feature of whose function in meroistic ovaries is to feed the boring larvae. eggs (Richards and Davies, 1988). The paired ducts Hymenopteran larvae, but not the sawfly cater- from the ovaries join medially to form a vagina pillars, are generally legless, move around only a into which lead ducts from the spermatheca and little and have a full set of small spiracles. The various accessory glands. After copulation, sperm is head capsule is entire but often less heavily scle- stored in the spermatheca, sometimes for long peri- rotized than in beetles. They are usually either ods. After fertilization, the accessory glands secrete parasitic or in cells being tended by adult females. diverse coverings to the eggs. The eggshell is termed Dipteran larvae are always legless. They have a the chorion and in harsh environments is complex large pair of posterior spiracles facing backwards and highly developed (Hinton, 1981). Fecundity may and looking a bit like eyes. The primitive larvae, as be measured as maximum potential fecundity (MPF) in crane flies and mosquitoes, have an entire head or achieved fecundity (AF). capsule with well-developed mandibles whatever But there is the question of identifying the juveniles. their lifestyle. The advanced ones are maggots, in Nymphs and larvae also attack plants and animals, which most of the head capsule has disappeared and one must know if they bite or suck. There are two and the mouthparts reduced to a pair of hook-like simple rules. First, since exopterygotes have no pupa mandibles. For discussion of ‘advanced larvae’, see (the stage of change), adult and juvenile mouth- McShea (1998). parts must be rather similar. Exopterygote nymphs Pupae are of course confined to the Endopterygota, usually look and often behave like small, wingless and potentially vulnerable by reason of their immo- versions of the adults. Second, all endopterygote bility. But this stage can sometimes wriggle, warding

General Introduction 7 (a)(a) ((b)b)

((c)c)

(d)) (e)(e)

Fig. 1.2. To identify endopterygote larvae use the following simple features: (i) The presence or absence of legs. In the former case their distribution on the larva. Boring larvae tend to have lost their legs through evolution. (ii) The presence or absence of a complete head capsule. (iii) The distribution of the spiracles (breathing holes opening into the tracheal system). (iv) Orientation of the mandibles. Insects with horizontal jaws (prognathy) are often carnivores, those with vertical ones (hypognathy) are generally herbivores. Detritus feeders are variable. (a) Coleoptera. Thoracic legs only, robust head capsule, complete set of spiracles, mandibles prognathous (carnivores) or hypognathous (herbivores). (b) Hymenoptera, Symphyta. Thoracic legs and more than four pairs of abdominal legs, robust head capsule, complete set of spiracles, hypognathous. (c) Hymenoptera, Apocrita. Larvae enclosed in a host or cell, legs absent, head capsule present, complete set of spiracles, mandibles variable. (d) Lepidoptera. Thoracic legs and four or fewer pairs of abdominal legs, robust head capsule, complete set of spiracles, hypognathous. (e) Diptera. Legs absent, head capsule in Nematocera only, with generally prognathous mandibles. Spiracles prothoracic and terminal on the abdomen. off attacks from parasitoids, or they are heavily 1968, 1998; Wilson 1998). First, individuals have sclerotized. Some braconid wasps pupate beneath different genetic structure resulting in different or around their dead victims, for example, Cotesia phenotypes. Second, a single genotype may exhibit melanoscela under gypsy moth larvae (Gross, 1993) variable phenotypes in different environments and Praon spp. under aphids (Richards and Davies, (Whitman and Agrawal, 2009). This is phenotypic 1988). Indeed, all ichneumonoid and moth pupae plasticity. But there are many characters for which are protected both from desiccation and from ene- such variation is discontinuous. For example, mies by a cocoon and sometimes by rolled up leaves. adults of the ladybird beetle, Adalia bipunctata, Butterfly pupae are exposed, but usually cryptically may be black or red; there are no intermediates. coloured (Section 1.5). Those of other groups develop Within several grasshopper species there are some in hidden places: in the soil, in wood or in hollow adults that are mainly green and others that are stems. mainly brown. In some parasitoids and water bugs there are short- and long-winged forms. Such discon- tinuous variation is called polymorphism and has 1.4.3 Phenotypic plasticity and been known for a long time (Reuter, 1875). Ford polymorphism (1961) gives a good formal definition: ‘Genetic poly- In populations of sexually breeding insects there is morphism is the occurrence together in the same considerable continuous variation between the indi- habitat of two or more discontinuous forms of a viduals of the same stage, that is, there are adap- species in such proportions that the rarest of them tive, individual differences between them (den Boer, cannot be maintained . . . by recurrent mutation’.

8 Chapter 1 We add to Ford’s definition only that the same during juvenile development in Bicyclus induces instar must be specified. Essentially, variation is the change in adult forms (Section 10.2.2.2). intraspecific and discontinuous (Harrison, 1980). A polymorphic population comprises morphologi- 1.4.4 Some further notes on insect cally distinct sub-units. All polymorphism has a classification genetic basis (Clark, 1976). Our definition excludes geographical races, continuous variation and rare Several insect orders end in the suffix ‘-ptera’, serving mutants that are normally removed by natural selec- to identify their ordinal rank. Therefore the order tion. Analysis shows, however, that if a morph Diptera comprises the ‘two-winged ones’ and the comprises as little as 1% of a population then it must order Lepidoptera contains the ‘scale-winged ones’. have some selective advantage, often only when Unfortunately, sub-orders have no reliable endings rare. In A. bipunctata the red forms survive the to identify them, but all is not lost because next winter better, whereas the black forms have a higher down the scale of classification, the superfamilies rate of increase (rm) during the summer. Mather all end in ‘-oidea’, the families all end in ‘-idae’, the (1955) showed that such polymorphism was the sub-families all end in ‘-inae’ and the tribes, if they outcome of disruptive selection (q.v.). exist, end in ‘-ini’. Students must learn these suffixes, Another conceptual angle on these different as I will not burden the text with explanations each forms is metamorphosis itself. The same individual time they turn up. They are also incorporated in exists in different forms in different instars. Both adjectives, for example, pentatomid bugs, culicine polymorphism and metamorphosis (Section 1.5) are, mosquitoes. In most plant families the equivalent of course, adaptations for different functions, as ending is -aceae. Lubbock (1874) and Reuter (1875) noted in Darwin’s Species are given two names in international biol- time. Again with respect to time, there may be sea- ogy. For example, a common blow fly has the scien- sonal changes in morph frequency, as in adult Adalia, tific name ‘Calliphora erythrocephala’. These names in some adult butterflies such as Precis (Mather, are always in Latinized form even if not actually in 1955), the tropical genus Bicyclus (Brakefield et al., Latin. Contrary to popular belief, this practice was 1996) and in adult flies such as Drosophila (Birch, started not by Linnaeus, although he certainly 1960). Two major polymorphic traits exist in developed the system massively by naming so many insects: (i) colour and pattern polymorphism; and plants and animals in this way. It was started in (ii) alary or flight polymorphism. For ecology, the the early seventeenth century by the Swiss botanist first relates in particular to survival (Section 10.2.3) Johannes Bauhin. Of course, back in those days but also to thermal relations, as in Adalia. The sec- everyone who was even slightly educated knew ond relates to movement, in particular to redistri- Latin anyway, so it is no surprise that scientific bution (Section 10.2.4). The latter affects: (i) variation names are in this erstwhile international language. in wing length; (ii) variation in flight muscle devel- Some papers are written giving the common English opment; and (iii) variation in flight behaviour name only. This is inadequate and often confusing: (Harrison, 1980). for example, there are two chrysanthemum leaf Although polymorphism always has a genetic miners (Section 5.2.2.1(a)) in different orders! And basis, in genetically determined polymorphism the to contract, say, the chrysanthemum leaf miner to environment has little or no modifying influence CLM, is even worse. It may save the printer’s time (Clark, 1976). In environmentally cued polymorph- but wastes the time of many readers, which is more ism or polyphenism (Mayr, 1963), the environment significant. Irritatingly, larval insects are often acts with the genotype to select alternative develop- popularly called worms with which they have an mental pathways resulting in different morphs extremely remote ancestry. Unfortunately, this (Moran, 1992a). Polymorphisms are due to genetic habit is too deeply entrenched to be extirpated, as differences between individuals. Polyphenic traits in the use of wireworm for elaterid larva. But in result from environmental differences acting on the some cases all is not lost: therefore Choristoneura same genotype, namely phenotypic plasticity. Such fumiferana is preferably called the spruce bud- causal cues are commonly crowding, an intrapopu- moth rather than the spruce budworm. The name lation effect, or temperature and food quality, which carries more useful information. Then for army- are factors of the wider environment. Crowding in worm the French term chenille legionaire is much the wasp Melittobia, and the ambient temperature more expressive.

General Introduction 9 Evolutionary change occurs at four levels: (i) species is recognized as a species complex: An. within populations; (ii) between populations, maculipennis sensu lato (= s.l., in the wide sense). where it may lead to: (iii) speciation; and (iv) Anopheles maculipennis sensu stricto (= s.s., in the macro-evolutionary levels, namely the formation of strict sense) is one of the sibling species comprising higher taxa such as genera and families (Wright, this complex, and so are An. sacharovi, An. 1982a; Maynard Smith and Szathmáry, 1995; see labranchiae and An. melanoon (Section 7.3.2.4(d)). Section 9.10). New species usually form when They may be distinguished morphologically, how- populations become reproductively isolated in ever, by the surface patterns of their eggs. Then, what was formerly a single species (q.v.). After spe- two sub-species of An. melanoon have been found. ciation the two resultant species will still have most Sub-species require three names, here An. melanoon of their genes and gene arrangements in common, melanoon and An. melanoon subalpinus. The sibling but in particular differ in genes that prevent inter- species of the An. gambiae complex are distinguished breeding. Through time, however, they will acquire by another criterion, the bands on their polytene several more genes that separate them further. The chromosomes. But what has led to great confusion gene pool records the species’ history. Even so, is that within the An. gambiae complex some of the because of conservatism in biochemical pathways a sibling species transmit malaria and others do not majority of genes are common to a wide range of (Section 7.3.2.4(d)). Molecular studies (Williamson, organisms (Section 9.1). For example, the gene 1992), however, are presently improving taxonomic McIr, which codes for melanin synthesis in mice, is resolution. But the problem is not confined to mos- believed to be similar to one in the melanic variety quitoes; it is far reaching. The biting gnat, Simulium of the moth Biston betularia, and the well-studied damnosum (Section 7.3.2.4(i)) is similarly com- shell colour and banding polymorphism in the land plex. Recently, it has been shown that the whitefly, gastropods, Cepaea nemoralis and C. hortenis are Bemisia tabaci (Section 5.3.1.2(c)), may comprise almost identical and have a similar genetic basis at least 24 morphologically inseparable species (Xu (Ford, 1975). Indeed, there are a large number of et al., 2010). major genes that are responsible for universal effects in organisms, plus an even larger number of 1.5 The Function of Insect Stages minor genes that code for the remaining variation (Fitzpatrick et al., 2005). It is fundamental that, because insects must shed Taxonomy is inevitably a continuing study. One their dead exoskeleton periodically in order to of the long-standing problems is species with mul- grow, they necessarily develop in a series of stages. tiple names. The same species has been described Through millions of years of evolution, and remem- more than once by different taxonomists, generally ber that insects pre-date the dinosaurs, these stages without either being aware of the fact. When this have been modified for several different biological has happened the name given first takes prece- functions as juveniles develop towards adulthood. dence. In detailed biological research the name of This is termed metamorphosis (Section 1.4.3). And the author, and sometimes even the year of descrip- as we have seen, these modifications, although not- tion, are appended to the scientific name, therefore able in aquatic palaeopteroids, are generally more helping to resolve the problem. But cryptic and extreme in the Endopterygota. sibling species are a nightmare. If in preliminary work In the egg stage, embryological development to two or more species are suspected, but not demon- the nymph or larva takes place. Usually this occurs strated, within an erstwhile good taxonomic one, after oviposition, but in some cases, for example in they are referred to as the former. Then later on, spe- blow flies, such development to the larva is nearly cies that have behavioural differences, are shown not complete at this time and hatching proceeds quickly. to interbreed in nature, but even so are morpho- In contrast, in some other groups the egg stage logically indistinguishable, at least as adults, are functions to bridge a period of harsh physical envi- referred to as the latter. Undetected sibling species ronmental conditions, such as drought (plague grass- (cryptic ones) are a source of confusion and error hoppers) or the depths of winter (temperate aphids, in both pure and in applied entomology (Walter, winter moths). In those species in which the egg stage 2003). Thus in the early days, one of the malarial spans a period of heat and dryness, the chorion is mosquitoes in Europe was called Anopheles macu- highly modified to resist desiccation while also lipennis, the spotted-winged anopheles. Today this allowing respiration to take place. The astoundingly

10 Chapter 1 detailed work by Hinton (1981) on this subject is movement may occur as the larvae age. Caterpillars and will remain a classic study. are sometimes gregarious when young but are later As we have seen, exopterygote nymphs in terres- solitary, like those of the white butterfly Pieris bras- trial situations normally function like miniature sicae and of the sawfly Nematus ribesii. Then, adults that are flightless and do not reproduce. They mature larvae often disperse briefly. This has two often share the same microenvironment with the main functions. First, centrifugal movement from adults, a feature much less common in endoptery- the feeding site results in a rapid decrease in popu- gotes (Bryant, 1969), who normally inhabit differ- lation density, that is, the number of individuals per ent juvenile and reproductive environments. But unit area (Sections 9.3 and 10.2.1). This means that while the primary function of the larva is to feed, it they become safer, since enemies have a more time- must also survive and may disperse. These larval consuming job searching for them. If several functions, in contrast to those of nymphs, are not mature larvae occupied a 1 m2 food plant and then restrained by the future functions for which adults moved up to 5 m from it to pupate, the initial pupal are selected, because the pupa allows for a total density would be about one-eightieth of the final restructuring. Therefore a caterpillar is primarily a larval density. This is an example of density- walking alimentary system. Just like a miniature dependent movement avoiding density-dependent cow, its relatively big gut is required to digest large mortality (Section 9.4). Against this potential gain quantities of poor quality food, usually with the must be set a possibly greater chance of suffering assistance of symbiotic microbes (Section 10.2.2.6). predation during dispersal. Second, larvae seek a During development the larva elaborates an extensive hiding place with a favourable microclimate for fat body, an energy and protein store of the build- pupation. Tsetse fly females retain and nurture a ing blocks from which to construct the adult. Even so, single larva in a uterus until it matures, then release such larvae, and especially those feeding externally, it at such a suitable site. employ a variety of devices to reduce predation and Exposed pupae, such as those of butterflies, are parasitism (Section 5.2.1.3(b)), that is, there are often cryptically coloured too. In some swallowtail also mechanisms for immediate survival. butterflies the pupae in a brood may be either green Coloration provides important survival strategies or brown, that is, there is cryptic polymorphism for exposed larvae (Section 5.2.1.3(b)). It commonly (Sections 1.3.3 and 10.2.3.5). This has two effects: blends in with that of the food material, reducing the (i) it allows the mature larva to seek a wider variety visibility of the larva to its enemies, a device called of backgrounds on which to pupate, indeed pupal cryptic coloration. A quite different strategy is to colour normally matches background colour; and sequester poisonous substances from food plants. (ii) it reduces the effective population density of The larvae doing this often use bright colours to pupae even further since potential predators treat advertise the fact that they are dangerous, a system green and brown individuals as different sorts of known as warning or aposematic coloration. prey. Moths usually have pupae concealed within Endophytic and soil-dwelling larvae, being hidden, silken cocoons, which the larvae spin with a secre- are often brownish or depigmented. In exposed lar- tion from their labial glands. Apart from affording vae, diurnal movement may also assist survival: some mechanical and physical protection, the movement and survival are linked. Cryptic larvae cocoon may also provide cryptic protection by normally feed only at night, therefore avoiding pre- incorporating fragments plucked from its immedi- dation from birds, lizards and the attention of most ate microenvironment. In the tropical, solitary mud parasitoids. Larvae that attack herbs frequently hide wasp, Trypoxylon palliditarse, late larvae spin a in the litter or soil below the plant during the day. cocoon and then put sand grains into its matrix, Older caterpillars of Lymantria (Section 5.2.1.4(f)) therefore constructing a barrier impervious to par- and the tropical, defoliating moth Melipotis move asitoids (Section 12.4). from the canopy of the tree at night to its base dur- In the juvenile stages of several pterygote insects, ing the day, but such cases are unusual for arboreal additional specialized stages may occur. Thus in species. Therefore, when the questing entomologist desert locusts the first nymphal instar is worm-like, finds fresh, biting damage to plants it is well to facilitating its ascent through the sand. The final search potential refuges for larvae. nymphal instar of mayflies is a dun, a stage adapted Apart from aerial dispersal in the young larvae of for escape from its aquatic environment. The first some forest moths (Section 5.2.1.4(c)), local dispersive larval instars of several endoparasitic wasps have

General Introduction 11 relatively huge mandibles, weapons providing a final When this occurs, for example, when entire proge- solution to superparasitism. These cases are referred nies develop in confined spaces, as in Melittobia to as hypermetamorphosis. Entomologists have (Section 8.2.2.1), females bias the sex ratio of their never been afraid of long words! progeny towards daughters (Hamilton, 1967). Now we look at the functions of the adult. First, Furthermore, several insect species are parthenoge- consider a few basic things about its gross anatomy. netic and in a few males are unknown. The MPF : Adult insects usually show a sharper division into female ratio varies according to species, from one the three body regions (head, thorax and abdomen) in some aphids to 10,000 or more in the Australian than do the juvenile stages, particularly in the swift moth Abantiades (Section 10.2.5.1), some endopterygotes. Morphogenesis proceeds in semi-­ tachinid flies and eucharitid wasps. independent compartments (Raff and Kaufman, Many tropical insect species have several genera- 1983, in Endler and McLellan, 1988). The head is tions per year, they are multivoltine. This also occurs the sensory and control centre, but also has the in several temperate species, such as blow flies. Here mouthparts, just like a vertebrate. The thorax is the different generations are subject to different selective locomotory centre. The abdomen is the visceral and forces, particularly from the physical environment reproductive centre. If one compares a blow fly (Moran, 1992a). As one moves poleward an increas- maggot with a blow fly adult the difference is very ing proportion of species become univoltine. Even clear. The maggot is effectively headless and has no so, in an inclement summer they may not be able obvious division between thorax and abdomen. to complete development. Nearer the poles many The adult has a well-defined head with complex species need more than a year to complete develop- mouthparts and diverse sensory equipment, includ- ment (Section 10.2.2.2). ing huge multifaceted eyes with ~240,000 neurones When a patch of food lasts only as long as the in the brain to process their information, antennae period of development, all emerging adults must with thousands of sophisticated sense organs, and so disperse to find a new one (Section 12.2.4), so all on. It has a thorax packed with flight muscles using adults should have similar flight capability. But where oxygen at a rate per unit mass similar to that of this patch lasts much longer, only some of them hummingbird wing muscles, and an abdomen with need to disperse, and we often find that the disper- a reproductive system that can produce over 500 sive capability of these adults is far greater than progeny in a week. The ensemble can deliver these that of those that stay. There is therefore a flight eggs to several suitable larval feeding sites kilometres polymorphism (Section 1.4.3). Consider the adults distant from each other and its natal environment. that disperse. A rough and ready relationship exists If we could construct a machine capable of this, one between an insect’s size and its speed of flight (air weighing <100 mg (a mini-drone), then we could say speed), namely all small insects are slow fliers, and fairly that we have reached the technological age. some large insects are fast fliers (Fig. 1.3) (Lewis The broad generality is that adult insects redistrib- and Taylor, 1967; Brackenbury, 1995), with speeds ute themselves (disperse or migrate, see below) first varying from ~0.5–10.0 m/s. Small insects cannot and the survivors seek resources and reproduce fly faster than a light breeze, so that they fly either afterwards. Exceptions are in a small minority. The near to the ground where the air speed is low and distance such individuals may travel varies from a hence may have some control over the direction of few metres to hundreds of kilometres. In the first case, their flight, or they fly up and let the wind carry many little Sternorrhyncha, such as psyllid bugs and them where it will. One can see that the spatial scale insects, redistribute themselves over several scale of these two modes is quite different. The first is generations within the same tree. But diminutive termed dispersal, the second, namely flight between diamond-back moths (Section 5.2.1.4(a)), which are habitats, is migration (Hassell and Southwood, not much bigger, may fly up into the clouds and be 1978). Small insects that undergo a long, largely transported hundreds of kilometres in a few days. passive dispersal high in the air, on finding food, In outbred species the numbers of the two sexes usually move only in a restricted ambit during are roughly equal (Fisher, 1930). As Clarke (1984) reproduction. Many aphids and the fruit fly do this. expressed it humorously: ‘The Almighty and Ronald Others, like clover weevils, lose their flight muscles Fisher between them decided that in general the once they have found the breeding site, hence ideal ratio between males and females should be becoming flightless and limited in their area of 1:1.’ But in inbred situations females predominate. operations.

12 Chapter 1 1000 800 600 400

200

100 80 60

Flight speed cm/sec 40

20

10 1.0 246810 20 40 60 80100 200 400 600 1000 Size (wingspan × length mm2)

Fig. 1.3. Flight speed and size in insects: all small insects are slow flyers, some large insects are fast flyers. Adapted from Lewis, T. and Taylor, L.R. (1967) Introduction to Experimental Ecology. London, UK: Academic Press. Redrawn with permission.

Medium-sized and large insects, especially in the density often has outcomes for the reproductive Hymenoptera, Lepidoptera and Diptera, are usu- success of individuals and, as a consequence, for their ally strong fliers and can progress against a moder- populations (Sections 9.4 and 10.1). ate breeze if they stay near the ground. By contrast, At the other end of the spectrum there are insects beetles are not normally strong flyers and also lack with very reduced mobility, such as scale insects, ocelli (Kalmus, 1945). Selection has promoted pro- that have been termed ‘plant parasites’. They lead an tection not speed. Honeybees, noctuid moths, big analogous life to, say, ectoparasitic lice on a mam- pierid butterflies and tabanid flies can fly up to mal in that the insects spend their entire life on a ~5 m/s (18 km/h) in still air. They have a high indi- single plant, living at its expense. But the obvious vidual searching capability (ISC) and never lose this difference is that their ‘host’ is not an animal. The capacity during reproduction (Section 10.2.4.1). comparisons that have been made regarding their Maximum speeds >10 m/s (36 km/h) are known for ecology (Price, P.W., 1997) are compelling, but they aeshnid dragonflies and hawk moths (Dudley, 2000), are the more so because one group attacks animals about the same speed as the world’s fastest sprinter. and the other attacks plants. Of course, these trophic Related to capability, they deposit their eggs in levels are not the same (Eggleton and Belshaw, 1992). several widely separated places. Placing eggs in sev- Rettenmeyer (1970) and Turner (1987) make a eral patches means that the female literally ‘does rather similar distinction when defining mimicry not put all the eggs in one basket’. A catastrophe (Section 10.2.3.5), excluding cases, under the head- befalling one egg batch will not kill all the eggs. ing of protective coloration, where insects resemble This strategy is termed ‘risk spreading’ and we refer plant parts or inanimate objects, for example, katy- to it again in Section 9.7. In effect, the female dids resembling leaves and moths resembling fae- reduces the overall population density of the pro- ces. Where insect herbivores become closely geny on a scale related to her ISC. Recall that while associated with their plant food (Price’s ‘plant para- the dispersal of larvae about to pupate has a similar sites’), as in many homopteroids, this leads to spe- ecological effect, they reduce their own population ciation and adaptive radiation with several parallels density (Sections 9.2 and 9.3). An odd case of redu- to ectoparasites. But some plants such as dodder cing population density of progeny is found in (Cuscuta, Convolvulaceae) and mistletoe (Viscum, dung beetles. Females roll their dung balls some Loranthaceae) live on and at the expense of other distance from their steamy site of origin. Population plants, and so are genuine plant parasites. Also

General Introduction 13 coming to mind are protists such as Phytomonas Pathogenic microbes infest both plants and ani- (Camargo, 1999). These have no connection to bugs mals, but there is little overlap in the taxa attacking such as scale insects. Therefore it is better not to these kingdoms. Two orders possessing piercing and attenuate the term ‘parasite’ and to separate it from sucking mouthparts, the Hemiptera (Exopterygota) ‘parasitoid’ and ‘micropredator’ (Section 7.1 and for plants and the Diptera (Endopterygota) for q.v.). Nor do I use the term ‘host plant’; here they animals, are the most important vectors. In Section are called ‘food plants’ as they always used to be. The 1.2 we distinguished biting from sucking insects, fact that plants provide facilities to insects other and exopterygote from endopterygote insects: than food is covered in the term ‘resource patch’ therefore basic taxonomy has consequences for (q.v.). As J.S. Kennedy (1953, in Dethier, 1954) puts pathology. Plants are immobile while most animals it, a food plant ‘is not merely something to be fed move actively: it may be no coincidence that on, it is something to be lived on’. Neither do I regard Hemiptera are the major vectors of plant pathogens, carabid beetles as occasional ‘seed predators’ (the while the more agile Diptera commonly transmit Short Oxford English Dictionary (SOED) defines pathogens that attack tetrapods. But this is conjec- prey as ‘An animal that is hunted or killed’). We ture (Section 11.5.1). know all these organisms transfer energy between the trophic levels and may share common biofacies 1.7 A Note for Students and co-evolutionary features. of Pest Insects Then there are practicalities. In describing biologi- cal interactions between a pest insect, its food plant Chapters 3 to 7 contain examples of pest insects and its parasitoids (tritrophic interactions), the selected for their importance and/or their interest, generic use of the term ‘host’ makes for difficult read- giving an idea of their global range, contrasting ing and can lead to ambiguity. For example, in a their ecologies and economic importance, and pro- paper by Preszler and Price (1988) entitled ‘Host viding a starting point for research. The list is far quality and sawfly populations: a new approach to from exhaustive. Even so, most of the pests have to life table analysis’, is the host the sawfly or its food be dealt with briefly. Much more is known about plant? Again, Kirk (1991) uses ‘host’ to refer to both all of these insects than can be given here. But so plants and animals. While the SOED also defines this that one can begin to appreciate the depth as well word generally, I think that in biology its use should as breadth of knowledge, certain pest species have be restricted to animals, otherwise the end point is to been highlighted. These were selected because: (i) have sheep viciously ‘predating’ pastures! Some I have personal field knowledge of them; (ii) they biologists would not agree with me, but see Hawkins are economically important; and (iii) taken together et al. (1990) and Speight et al. (1999, p. 88), who do. they illustrate a contrasted range of ecologies and are used as examples in the ecological chapters (Chapters 9 to 12). At the other end of the scale, a 1.6 Insects as Vectors and Pollinators few less important but related pests may be named Insects, being mobile and a handy size, are frequently at the bottom of the section on a main pest. Hence, employed by less mobile organisms to seek and find we deal with pests on three levels of detail: high- new requisites. Pathogenic microbes exploit them lighted, basic and additional. More comprehensive to find new hosts; flowering plants do so to distrib- lists appear in Hill (1997) for world pests and in ute pollen (male gametes). While microbes, unless Pedigo (2002) for North American pests. The pests symbiotic, do not reward insects for their services, of vegetables are covered in McKinlay (1992). flowering plants usually do (Section 8.2.1.1). The Two general points remain. The spatial scale on best that microbes usually do is to interfere mini- which a pest operates depends both on its numbers mally with an insect’s ability to seek and find req- and on its redistributive capability. For medical and uisites, thereby furthering their own imperatives veterinary pests, area-wide control is an ideal. Plant (McNeill, 1976). But symbiotic microbes may pests operate on a variety of scales. Locusts and improve growth and defend insects in various ways aphids, for example, operate on vast scales, as bil- (Section 10.2.2.6). And with phytoplasmas (Section lions of individuals can migrate hundreds of kilo- 5.3) there is evidence that infection can improve the metres. Colorado beetles and gypsy moths operate vector’s reproductive success. All of these are prob- on a scale of only a few kilometres. But the scales ably co-evolved situations. on which we deal with plant pests are essentially

14 Chapter 1 horticultural and agricultural ones. Horticulture agriculture, we deal with spaces measured in tens means ‘culture in gardens’ (Latin: hortus – a garden), of hectares, so mass methods must be employed. while agriculture means ‘culture in fields’ (Latin: The culture of vegetables was largely within the ager – a field). In the former we deal with a con- province of horticulture, but over the past decades fined space, the garden, in which each plant can get more and more of them have been grown on an individual attention from the gardener. The word agricultural scale. This yields a cheaper product, ‘orchard’ comes from the Old English ‘ortgeard’, albeit with for various reasons some reduction of and the ‘ort’ bit probably comes from ‘hortus’. In quality, as you may have noted!

General Introduction 15