Plant-Insect Interactions PDF

PLANT - INSECT INTERACTIONS Dr. LUP Heshula  Course Outline: Twoweeks lectures (i.e. on fundamentals): Week one (): Overview of Insect-plant interactions. Types of insect-plant interactions. Plant defences to insects feeding. Plant fitness in defences. Week two (): Insect pre-adap...

PLANT - INSECT INTERACTIONS Dr. LUP Heshula  Course Outline: Twoweeks lectures (i.e. on fundamentals): Week one (): Overview of Insect-plant interactions. Types of insect-plant interactions. Plant defences to insects feeding. Plant fitness in defences. Week two (): Insect pre-adaptation or adaptation to plant association. Pollination. Insects as weed biocontrol agents. Host plant resistance.  Recommended readings Bernays, E. A. & R. F. Chapman. 1994. Host-Plant Selection by Phytophagous Insects. Chapman & Hall. Gullen, P. J. & P. S. Cranston. 2005. The Insects. Blackwell Publishing. Chapter 11. Schoonhoven, L. M., J. J.A. van Loon, & M. Dicke. 2005. Insect-plant biology. Oxford University Press. Strong, D. R., J. H. Lawton, & R. Southwood. 1984. Insects on Plants: Community Patterns and Mechanisms. Blackwell Scientific. Waser, N. W. & J. Ollerton. 2006. Plant-pollinator interactions: from specialization to generalization. University of Chicago Press.  Outcomes Exhibit a fundamental understanding of the basic features of plant-insect interactions and complexity of ecological interactions in general. Exhibit a basic understanding of how ecological interactions may affect biological diversity over evolutionary time. Exhibit an understanding of how knowledge of ecological interactions between insects and plants can be used to improve pest and weed management. Demonstrate critical thinking. Why study plant-insect interactions? 1. Plants and insects are the most diverse and abundant organisms. 2. Plant-insect systems are crucial links in maintaining diversity and abundance of all life. 3. Plant-insect systems are great models for testing ecological and evolutionary theory. 4. The greatest competitors of humans are phytophagous/herbivorous insects. 5. Herbivorous insects can be used as biological control agents against weeds.  Gullan and Cranston 2005 Insects > 1million Plants > 320 000  300 million year old herbivory Piercing-sucking insect damage Stylet tracks Gall on petiole of a a tree fern Damage from boring insects from Labandeira 1998 Types of interactions between plants and insects: Ecological: Herbivory Pollination Seed predation Seed dispersal Indirect (through competition, higher trophic levels) Evolutionary: Specialization Speciation Coevolutionary: -Pair-wise; reciprocal adaptation (arms races); insect ability to detoxify poison produce by plant - Guild/co-phylogeny; flowering plants and pollinating insects.  General types of ecological interactions and their outcomes Type Consequence partner 1 partner 2 competition* - - parasitism / predation* - + mutualism* + + commensalism? 0 + amensalism? - 0 - * Directly relevant to plant-insect interactions ? May occur in plant-insect interactions Herbivorous (phytophagous) insects can be classified based on effects of insects on plants as follows: 1. Chewers tear and bite off plant tissue with sharp mandibles. 2. Sap suckers probe into plant tissue with piercing- sucking mouthparts (mandibles, labium) modified to take up liquid like sipping through a straw. 3. Miners burrow through leaf tissue creating tunnels of eaten tissue. 4. Gallers transform plant tissue into domiciles in which they feed and develop. Herbivorous insects can be classified by where they feed: 1. Ectophytic insects feed externally. 2. Endophytic insects feed within plant tissue. Chewing insects may have characteristic feeding behaviors.  A true bug (Hemiptera) using its piercing-sucking mouthparts proboscis Leaf miners are endophytes... …and may also have characteristic feeding behavior Leaf mines: a) linear-blotch on elm leaf; b) linear mine on primula leaf; c) linear blotch mine on gentian leaf; d) linear mine on ragwort leaf; e) blotch mines on apple leaf; f) linear mine on poplar leaf; g) blotch mine on jarrah leaf from Gullan & Cranston 2005 Herbivorous insects are also often classified by the range of plant taxa they feed on: 1. Monophagous species feed on a single host plant species genus, or family, depending on the researcher’s focus. They are specialists. 2. Oligophagous species feed on a limited number of host plant species, genera, or families. They are fussy, but not that fussy. 3. Polyphagous species feed on a wide range of host plant taxa. They are generalists.  You can see that this is really a continuum: Monophagous 1. Monophagous species feed on a single host plant species genus, or family, depending on the researcher’s focus. They are specialists. 2. Oligophagous species species on a limited number of host plant species, genera, or families. They are fussy, but not that fussy. 3. Polyphagous species feed on a wide range of host plant taxa. They are generalists. Polyphagous This caterpillar of the pipevine swallowtail butterfly which feeds exclusively on pipevine plants. It is monophagous. The golden tortoise beetle is associated with sweet potato and related species such as morning glory, Ipomoea spp.; and bindweed, Convolvulus spp. Only plants in the family Convolvulaceae are hosts. It is oligophagous. On the other hand, many grasshoppers will eat just about anything. They are polyphagous. In spite of the incredible diversity and abundance of phytophagous insects, the world is a green place. Plants continue to thrive. Why? WHY IS THE WORLD GREEN? Hairston, Smith & Slobodkin in 1960 hypothesized that predators kept herbivore numbers low enough to prevent wholesale depredation of plants. This marked the beginning of a long and continuing debate in ecology over whether “top-down” (higher trophic levels) or “bottom- up” (primary producers) factors regulate herbivore populations. The hypothesis assumes that all this green stuff is edible. Hairston, N.G., F.E. Smith, & L.B. Slobodkin 1960. American Naturalist 94: 421-425. Plants pose some serious challenges for insects. In general, these involve: attachment; insects must gain and retain hold on plants in order to feed. desiccation; exposed insect may be subject to greater desiccation than aquatic/litter dwelling insects nutrition; diet of plant tissue is (except seeds) is nutritionally deficient in proteins, sterols, vitamins. plant toxins; repellents, poisons, reduce digestibility, adverse effect on insect behavior/physiology. protective structures; sclerophylous tissue, spines, spicules Attachment  Dessication NBfor insects that live on the exterior surfaces of plants e.g. Orthoptera, Lepidoptera, and Thysanoptera morphological behavioural physiological  Nutrients: how edible are plants? Digestibility of plant constituents Animals lack the enzyme (cellulase) needed to degrade much of the cell wall components. from Iason & Van Wieren 1999  Low concentrations of nitrogen in plants means it is often limiting for insects. from Strong et al. 1984. Insects on Plants Seems better to be a predator, and better to eat some plant parts more than others. The major points about nutritional value of plants: 1. Plants are a relatively poor source of nutrition. 2. Plants vary among plant parts, and among individuals, populations, and species in nutritional value. 3. Plants vary across time in nutritional value. 4. Insect herbivore behaviours, life histories, and evolution are strongly influenced by this variation. Plant toxins and protective structures Leaf surface interactions 1st physical contact between an insect and a plant Zygogramma sp. - Leaf Beetle Chrysomelidae Plant toxins and protective structures The plant surface: Stems, shoots and roots often have thick bark composed of suberin, lignin, and cellulose. from Raven et al. Biology of Plants. 1992 The plant surface: The leaf cuticle is composed of pectins, fibrous materials, and is covered by a waxy layer. Juniper, B. & T. R. Southwood. 1986. Insects and the Plant Surface. Plants defend themselves! Types of plant defense: mechanical chemical indirect defense life history Mechanical defense: Besides wax coverings, plants are armed with spines, thorns, sticky glands, etc. Some plant epidermal cells differentiate into complex structures called trichomes.  Some examples of trichomes Vesiculate trichome Simple trichome Stellate trichomes Peltate trichomes Juniper, B. & T. R. Southwood. 1986 Leaf wax, trichomes, and other structure of the leaf surface may have a number of roles: 1. prevent desiccation 2. prevent UV damage 3. as an adhesive for climbing plants 4. as a defense against insect herbivores Trichomes can inhibit herbivory. These arthropods have been caught in the sticky exudates of trichomes. Juniper, B. & T. R. Southwood. 1986.  Many plants contain gummy substances that inhibit herbivore access, or are toxic. The latex seen here on a poppy capsule can obstruct insect feeding. Note: the chemical found in opium did not evolve to get humans high. Pines and other conifers have canals which they secrete resins into. Both the number and amount of resin increases upon wounding. before wounding after wounding Types of plant defense: mechanical chemical indirect life history  Physiological host range: Range Insect host ofrange plants that insect is capable of feeding & developing on under artificial (lab) conditions in absence of choice. Determined by laboratory host-specificity tests. Ecological (true) host range: Range of plants that insect actually feeds & develops on under natural (field) conditions when able to choose. Determined by field studies is usually much narrower than physiological host range. Physiological vs true host range Several agents for Solanum weeds feed & develop on cultivated eggplant (Solanum melongena) during lab trials. None are reported to attack the crop in their countries of origin. Silverleaf nightshade Bugweed Chemical defense: Plants have a range of morphological features that can act as defenses. Chemicals have provided plants with a plethora of defenses against the onslaught of ubiquitous herbivores. Plant chemicals may have different effects: repellence; volatiles - various compounds. reduced digestibility; phenolics, tannins, proteinase inhibitors. toxicity; alkaloids, cyanogenic glycosides. Glandular trichomes; secrete sticky substances or toxic chemicals. Juniper, B. & T. R. Southwood. 1986. Insects and the Plant Surface.  Wild potato and other plants in the family Solanaceae have 2 trichome types (Type A and B). Type A Type B (tetralobulate) (simple) Plant secondary chemistry Plants have a bewildering array of chemicals that seem to have little use in the general maintenance and reproduction of the plant ( = primary metabolism). For this reason, they have been called “secondary chemicals” Secondary plant substances Plantcompounds that are not universally found in higher plants, but are restricted to certain plant taxa, or occur in certain plant taxa at much higher concentrations than in others, and have no (apparent) role in primary metabolism. >100 000 identified compounds. The chemical world a phytophagous insect finds itself in is exceedingly complex. Many secondary chemicals are nitrogen (N) based. Includes many familiar plant derived substances such as nicotine, cannabis, caffeine, etc. but also a host of others (these are alkaloids).  The class of plant chemicals known as alkaloids are toxic to animals in general. This is what killed Socrates (hemlock) Deadly Nightshade (Atropa belladonna) – Used by wife of Emperor Augustus against foes! from Harborne 1992  Plant chemicals exhibit defences in two ways; 1. Qualitative defences; Highly toxic nitrogenous chemicals that are effective at low doses. 2. Quantitative defences; Large carbon-based chemicals with effects that depend on dose. Milkweeds (Asclepias spp.) produce multiple chemicals called cardiac glycosides. They are toxic to most insects. from Harborne 1992 …but not these Papilio dardanus Male Male-like Papilio female of dardanus Papilio dardanus Palatable Unpalatable mimetic forms of Danaidae female Papilio dardanus Plant defense may be: Direct defense – plant traits that affect herbivore directly. Indirect defense – plant traits that affect herbivores by attracting natural enemies, or affecting outcome of competition between herbivores. Examples of indirect defenses: Domatia – clusters of hairs in axils of leaf veins that provide predatory mites with shelter; hollow thorns of acacias Attraction of herbivore natural enemies – Extrafloral nectaries – provide supplementary energy supply to ants that protect plants. Volatile organic compounds – attract natural enemies of herbivores; stimulate neighboring plants to produce defensive chemicals. Domatia are not induced by the inhabitants  Effect of predators on mites w/wo domatia Orthotydeus lambi Amblyseius andersoni Norton et al. 2001  Domatia on Acacia domatia From Gullan & Cranston 2005 Acacia sphaerocephala Kibara, Myzolecanium kibarae, and Pseudomyrmex ants and Anonychomyra scrutator  Volatile organic compounds attract parasitoids Baseline level of volatilization increases after wounding In some cases insect may secrete an “elicitor” chemical from Pare & Tumlinson 1999  Species specific signaling Catepillar damaged & undamaged control plants Catepillar damaged & undamaged controls with larvae and damaged leaves removed Heliothis virescens (HV) is host of the parasitoid Cardiochiles nigriceps. HZ = Helicoverpa zea from De Moraes et al. 1998 Blend of volatiles differs between herbivore species and undamaged plants Gas chromatogram – numbered peaks are significantly different from De Moraes et al. 1998 Plant recruitment of predators and parasitoids Compounds released after wounding differ from those produced constitutively. Released compounds are not stored in plant but synthesised de novo. Volatile compounds are released by undamaged leaves of damaged plants (defence is systemic). The blend of compounds released can be specific to a given herbivore. Expression of plant defense: constitutive defense - plants produce defenses constantly induced defense – plants produce defenses only when attacked  If defenses cost the plant in terms of resources not devoted to growth and reproduction, etc. “turning on” the defense only when needed should be beneficial. Induced defence may be: Rapid induced defences – expressed within hours after damage Delayed induced defences – expressed in season after damage Types of plant defence: mechanical chemical indirect life history Life history strategies and plant defense: plants can prevent or reduce insect attack by escaping in space or time. Plants can escape in space by being small, cryptic, or surviving in inhospitable environments. Plants escape in time - by focusing effort to growth and reproduction at times when herbivores are not present or are less active, - by focusing growth in short pulses, or - by completing the life cycle rapidly. Costs of plant defense: Does defense (morphological structures, secondary chemicals, extrafloral nectaries, even life history traits) carry a cost to the plant? (The currency is fitness.)  A model of plant allocation of resources Resources allocated to D reduce resources to G. from Karban & Baldwin 1997 Measuring costs of defense: Estimate fitness of resistant and susceptible plants in the absence of damage as well as in the presence of damage (inoculate herbivore, or simulate damage). Measuring costs of defense: damage Fitness of resistant plants no damage Fitness of susceptible plants damage no damage S plant S plant fitness fitness R plant R plant damage no damage damage no damage Costs No costs Results have been mixed. Costs? + + - - + - - + + + from Simms 1992 Can plants compensate for damage by herbivores? Undercompensation – damaged plant produces less than controls. Compensation – damaged plant makes up for it’s losses, production equal controls. Overcompensation – damaged plant produces more than controls. Indirect effects of plants on competition between herbivores: induced resistance may intensify competition (immediate effect of induction). early season herbivores may reduce plant quality for later arriving herbivores (delayed effect of induction). early season herbivores may facilitate later arriving herbivores (induced susceptibility). decreased nutritional value under herbivory may intensify competition. Herbivore Offense: Insect adaptations (or preadaptations) to plant association are: physiological / biochemical behavioral morphological sensory Physiological adaptations: Insect guts have detoxifying enzymes: esterases P-450 cytochrome monooxygenases These enzymes metabolize many plant chemicals, often by converting non-polar compounds into polar compounds - makes it easier to excrete them. Example: The parsnip webworm (Depressaria pastinacella) is a specialist on parsnip. Parsnips contain high levels of the chemicals furanocoumarins, which are highly toxic to most herbivores. The parsnip webworm uses an enzyme, cytochrome P-450 monooxygenase, to metabolize furanocoumarins. The furanocoumarins are oxidized from a lipophilic compound to a hydrophilic compound, which can easily be eliminated from the body. Insects may have help. Many insects have managed to feed on nutrient poor diets (high cellulose, phloem sap, xylem sap). How do they do this?  Some symbioses in insects. Plant feeders  Behavioral adaptations: circumventing plant defense by sabotage trenching avoiding Some catepillars have been found to cut down trichomes before feeding (Hulley 1988). Trenching latex exuding plants (milkweed) Behavior: More ways insects can overcome or avoid the chemical and nutritional challenges that plants pose: 1. Gregarious feeding (Lepidoptera, Coleoptera, Homoptera) - creates nutrient sink or overcome defenses. 2. Concentrate feeding when nutritional values are highest and/or defensive chemicals lowest. 3. Concentrate feeding where nutritional values are highest and/or defensive chemicals lowest. 4. Increase utilization rates Gregarious feeding S. Hight Feeding where defensive compounds are low Insects sometimes use plant secondary compounds for functions other than nutrition or host recognition: Insects may sequester these compound in their body which renders them toxic to predators (many others besides Monarch). Insects may use these compounds as precursors of pheromones. Pollination Halictid bee photo by Alex Wild The insect-plant association is over 300 million years old - the evolution of the flower opened up a whole new world of interactions. Sphingid moth photo by Alex Wild The flower is a finely-honed attraction and dissemination device for fitness maximization, i.e., pollen dispersal. Some general considerations: Pollination by insects (entomophily) may be passive, or active. Many but not all flowers offer insects “rewards” for their services. Pollination by wind (anemophily) is usually considered to be ancestral, but may be secondarily derived. Flowers are “designed” for particular pollination strategies. Advantages of entomophily over anemophily: 1. increased efficiency of pollination. 2. successful pollination when wind unsuitable. 3. specificity (even rare plants receive conspecific pollen). The vast majority of insect pollinators come from 4 orders: Hymenoptera ~ 47 % Diptera ~ 26 % Coleoptera ~ 15 % Lepidoptera ~ 10 % Thysanoptera ~ ??  Flies as pollinators Fliesare irregular and unreliable pollinators but their abundance and the presence of some species throughout the year make them important. Fly-pollinated flowers are usually not showy, but often have a strong smell. Most flies visit flowers for nectar. Flesh fly on a mango inflorescence; photo by Dennis Anderson Hover fly photo by Alex Wild, UCD The carrion flower, Stapelia gigantea, smells like… native to South Africa Flies as pollinators (continued) Philoliche aethiopica Drakensberg, South Africa Photo by Alex Wild, UCD  Lepidoptera as pollinators Most species have a long, thin proboscis and feed on flower nectar From: Gullan & Cranston (2000) Flowers pollinated by butterflies or moths are often tubular and sweet- smelling. Butterflies visit flowers by day and moths usually at dusk or during the night.  Hymenoptera as pollinators Wasps may be generalist or specialist pollinators. Bees are probably the most important pollinators. Ants often visit flowers but are poor pollinators: they rarely cross-pollinate & secretions from glands on their body may kill pollen.  Wasps as pollinators (continued) These wasps are specialist pollinators of orchids, whose flowers mimic the appearance and odor of the female wasp and trick the male wasp into copulating with the flower. Orchid flower - looks like a Female “super” wasp Male female wasp on wasp flower of a second orchid sp. Ophrys insectifera Gorytes mystaceus orchid pollinia next flower  Bees as pollinators Bees collect nectar and pollen for their brood (larvae) as well as for their own consumption. Over 20,000 bee species worldwide and all are flower visitors.  Bees as pollinators (continued) Plants that depend on bee pollination often have bright (yellow or blue), sweet-smelling flowers with nectar guides (lines or colors, usually invisible to us, that direct the insect to the target nectar). from Purves et al. (1995) Life. The Science of Biology  The honey bee, Apis mellifera The main bee pollinator worldwide. Extremely important for many crop plants. A. mellifera is native to Europe but has been carried everywhere by people. But honey bees can cause serious problems in natural ecosystems - (1) they compete with native insect and bird pollinators for nectar & pollen, and (2) they may disrupt pollination of flowers by displacing specialist pollinators. Ecological effects of bees Individual honey bees quickly deplete the pollen from flowers from Paton (1993) Ecological effects of bees Many bees, including native carpenter bees, rob flowers of nectar without pollinating from Frankie & Thorp (2003) Some intimate interactions: Figs and fig wasps. Cycads and beetles. Both are examples of what is known as nursery pollination where insects lay their eggs into the reproductive structures of the plant. When insect herbivores are friendly: weed biocontrol What is a weed? A plant that is in the wrong place at the wrong time. What is an invasive weed? A non-native weed that is displacing native species and disrupting native and/or agricultural ecosystems. What makes organisms invasive? 1. better competitors. 2. able to flourish in human disturbed habitats. 3. escape from natural enemies. Most weeds become invasive partly due to lack of natural enemies (herbivores): Plants may be kept in check in native ranges by herbivores. Herbivores in introduced range often don’t attack. The premise of biocontrol: Pests and weeds are invasive species. Invasive species have lost their natural enemies. (Enemy release hypothesis). Introduction of natural enemies will restore control. Host specific natural enemies can be found in the native range of the pest / weed.  The goal of weed biocontrol: reduce weed density to acceptable level Agents are imported from weed’s country of origin to restore balance - Classical biological control. Agents don’t eradicate weeds but lower their densities below damage threshold (level where they cause problems). Native vegetation recovers due to less competition from weed. Manipulating plants by selection and breeding: In early agriculture plants were improved by “unconscious” selection: Most pest tolerant and best producers donated the most seeds for next years crop. Result was gradual improvement in both agronomic and resistance (defence) characteristics. Active breeding selected for agronomic characters at the expense of resistance characters: resistance was lost unintentionally. resistance was intentionally bred out as undesirable  Cassava plants have high levels of starch in roots, but also high levels of cyanogenic glycosides.  Now bred for sweetness and low levels of CG’s Crop plants that tolerated or escaped insect attack were noted as early as the 19th century. High levels of insect attack, overuse of insecticides, and evolution of resistance to insecticides in the mid-20th century made breeders look more actively for plant resistance to insects. Host Plant Resistance (HPR): It is clear that plants defend themselves against herbivore attack. To the extent that they do so they are said to be resistant. Entomologists and plant breeders have utilized plant defence in a management tactic called Host Plant Resistance. Host plant resistance has been classified into 3 main types: 1. Antibiosis – leads to increased insect mortality, reduced fecundity. 2. Antixenosis – leads to behavioral avoidance of plant. 3. Tolerance – herbivory unaffected, plant suffers no loss of fitness or yield. Painter, R. H. 1951. Insect Resistance in Crop Plants. Host plant resistance has been classified into 3 main types: 1. Antibiosis – caused by nutritional deficiency or toxicity. 2. Antixenosis – caused by disruption of host selection. 3. Tolerance – caused by compensation or overcompensation. Painter, R. H. 1951. Insect Resistance in Crop Plants. Sources of resistance: existing variants within crop / population. search among cultivars and germ plasm collections. wild progenitors or relatives of the crop plant.