Species Interactions III Herbivory

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Species Interactions IIIHerbivory
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Outline

• Definition Focus on insects
• Characteristics of invertebrate herbivores
• Fossil history
• Types of insect feeding
• Nutritional requirements
• Nutritional obstacles
• Plant defenses 1. Physical 2. Chemical
• Herbivore responses
• Herbivore specialization
• Herbivore diversification
• Coevolution
• Ecological impacts of herbivory

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Herbivory

• consumption of plants by animals
• Basis of all food chains, important
• for fundamental ecosystem processes
• like nutrient cycling
• Seed seedling herbivory more
• like predation i.e. individual plant
• is often killed outright
• Herbivores that feed on leaves or other plant
  parts usually do not kill the plant but can
  reduce growth reproduction
• When herbivory is lethal - generally takes quite
  a while
• Herbivores can feed externally (leaf, bud,
  flower feeders) or internally (leaf miners,
  gallers, stem borers)

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Invertebrate herbivores

• Differ from vertebrate herbivores in their size,
  numbers, and the type of damage inflicted
• Invertebrate herbivores often have a lifelong
  association with a plant (due to small size)
• Short generation times --gt rapid rates of
  evolution
• Invertebrates generally more specialized than
  vertebrates

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History of herbivory

• Plant-insect interactions common in fossil record
• Evidence of herbivory since Paleozoic (400 mya)
• All insect feeding types except leaf-mining
  established by Late Pennsylvanian (300 mya)

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Types of insect feeding

• Chewing
• Lepidoptera (160,000 named species) almost
  entirely herbivorous, larvae are mainly leaf
  chewers, adults feed on nectar
• Orthoptera (20,000 species)
• Coleoptera (350,000 species)
• Hymenoptera (150,000 species), also include
  pollen and nectar feeders

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• Sucking
• Hemiptera (112,000 species) sucking mouthparts,
  feed on plant sap
• aphids (feed on sugar-rich, protein-poor plant
  sap, consume excess sugars for their needs,
  excrete excess as honeydew via anus)
• Superfamily Cicadoidea, feed on xylem sap eg
  17-yr periodic cicadas, spittle bugs
• Whiteflies, feed on contents of mesophyll cells

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• Gall-making
• Gall makers manipulate host tissues to provide
  themselves with rich source of nutrients and a
  protective shelter.
• Females lay eggs in specific part of plant,
  induces plant tissue around eggs to divide very
  rapidly, produces a gall.
• Larvae emerges from gall as an adult.
• Galling has evolved many times, common way of
  life amongst wasps, flies, aphids and thrips

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• Leaf-mining
• Female lays eggs in or on leaf
• Larvae develop through most or
• all instars within leaf
• Emerge as adults
• Miners vulnerable to predation
• parasitism while in mine
• Also vulnerable to leaf drop

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Nutritional requirements of insect herbivores

• All animals require fats, proteins, carbohydrates
  , vitamins and mineral
• Insects cannot synthesise essential amino acids,
  sterols, linolenic acid and vitamins, must obtain
  these from food
• Digestive process
• Saliva, containing digestive enzymes such as
  amylase secreted by labial glands
• Food passed to foregut, may act as temporary
  storage area
• Bulk of digestion occurs in midgut, digestive
  enzymes (proteases, lipases and carbohydrases)
  convert complex nutrients into simpler compounds.
  Most digestion and detoxification of harmful
  chemicals occurs here
• More water and nutrients absorbed in the hindgut
• Waste frass eliminated from rectum

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A big ecological question Why is the world green?
Herbivores rarely consume all plant resources
available, why not?

• 1. Herbivore populations limited by other factors
  (eg weather, predators, competitors) rather than
  by food availability (top-down vs bottom-up
  regulation)
• 2. Not all plant food is available for herbivores
  
• Herbivore chemical composition different from
  plants, many components of plants are
  indigestible
• (ii) Plant defend themselves

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• Plant-feeding insects live in a world dominated
  on the one hand by their natural enemies and on
  the other hand by a sea of food that, at best, is
  often nutritionally inadequate and at worst is
  simply poisonous
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  Lawton McNeill (1974)

The small fraction of insect orders that have
adapted to feed on green plants is remarkable
because plants are the most obvious and readily
available food source in terrestrial
communitieslife on higher plants is a formidable
evolutionary hurdle that most groups of insects
have conspicuously failed to overcome.

Strong et al. (1984)
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Nutritional obstacles for herbivores

• Ecological efficiency
• Only about 10 of plant material available to
  next trophic level (ie herbivore).
• Partly due to presence of indigestible
  compounds such as cellulose and lignin.
• Some insects house symbiotic bacteria
  that can digest these compounds

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Nutritional obstacles (cont)

• Chemical composition of plants and herbivores
  dissimilar. In particular, protein in short
  supply in plant material nitrogen content of
  leaves typically 2, but 30-40 of insect tissue
• Some herbivores can increase their consumption
  rate in response to N-content of plant tissue eg
  xylem feeders can consume 100-1000 times their
  body weight per day because amino acids comprise
  only tiny proportion of the sap
• Plants may protect their N in the form of
  non-protein amino acids that are toxic (many are
  neurotoxins)
• Micronutrients such as Na may also be in short
  supply in plant tissue (Na is 2.5 x higher in
  animal tissue than plant tissue, insects like
  butterflies compensate by feeding on salt in
  mineral licks, animal urine, bird droppings, male
  moths incorporate large amounts of Na in their
  sperm packets - part of nuptial gift to female
  during mating)

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Nutritional obstacles (cont)

• 3. Distribution of nutrients seasonally and among
  plant parts
• Macro-and micronutrients distributed unevenly
  among plant parts so herbivores often adapted to
  feeding on a subset of the plant
• Different types of feeding apparatus can also
  limit plant parts used eg mouthparts adapted for
  sucking phloem or xylem sap cant be used to chew
  leaves
• Many plant parts (eg fruits, flowers, pollen)
  only available for limited parts of the year
• Age of plant part also affects feeding eg young
  leaves more nutritious than mature ones

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Plant defenses against herbivory

• I. Physical defenses
• Tough epidermis, may prevent feeding, or induce
  mandible wear
• Cuticular deposits, wax, sticky resins
• Spines, thorns, prickles, stinging hairs
• Strategic (eg placement of meristems,
  underground reproduction

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Physical defenses (cont)

• Bursera schlechtendalii shrub native to Mexico
  Guatemala
• Squirt gun defence
• Possesses a network of pressurized terpene
  canals
• When canal is severed by a herbivore, shoots a
  stream of terpenes up to 150 cm
• Defence effective against many but not all
  herbivores
• Chrysomelid beetles in genus Blepharia can still
  feed on shrub, experiences only slightly reduced
  growth on only the most responsive plants

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Physical defenses (cont)

• Abscission defence plant drops leaves infested
  by herbivores
• Effective against relatively immobile herbivores
  such as leaf miners
• Can be costly to plant due to loss of
  photosynthetic area and stores of nutrients

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Physical defenses (cont)

• Third party defence Eg. Ant-acacias
• Acacia ant Pseudomyrmex ferruginea and closely
  related species actively defends Acacia host form
  other herbivores and clear away surrounding,
  competing vegetation
• In return, plants provide ants with swollen
  thorns in which to nest, plus carbohydrates from
  Beltian bodies and extrafloral nectaries
• Potential disadvantage is that potential
  pollinators may also be repelled its been
  found that a chemical signal produces by the
  flowers during pollen production repels ants

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Plant defenses against herbivory (cont)

• II. Chemical defenses
• Production of toxins, repellents, anti-feedants
• Secondary metabolites generally derived from
  metabolites involved in primary physical
  processes such as respiration, photosynthesis etc
• Many have medicinal value
• These compounds were traditionally regarded as
  waste products
• Fraenkel (1959) seminal paper discussed idea
  that they were herbivore defenses

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Plant toxins

• All green plants have the potential to be toxic
  to herbivores
• Toxicity dependent on
• Dose taken over time
• Age health of herbivore
• Mechanism of absorption excretion
• Detoxification system
• Not all parts of plants necessarily toxic
• Fruits usually toxin free
• Seeds usually protected

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Major classes of plant toxins
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Plant toxins (cont)

• Many secondary metabolites have multiple
  functions
• Eg.
• Alkaloids repel or deter herbivore feeding but
  are also used in antimicrobial defense
• Phenols protect against UV damage
• Secondary metabolite production is costly
• Eg.
• Production of N-based compounds can be limited
  by N-availability
• Despite presence of defensive compounds most
  plants are fed upon by a suite of specialized
  herbivores adapted to use these compounds as
  attractants, feeding stimulants or as a source of
  toxins for use in defense against enemies

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• Third party defence
• Other groups of organisms may be involved
• Eg Fungal endophytes live inside plants, produce
  toxins such as the ergot alkaloids

• Endophyte of tall fescue (Festuca arundinacea)
  produces toxic alkaloids that result in gt600
  million worth of livestock losses in US p.a.

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Plant defense mechanisms

• Constitutive defenses
• Defense mechanism is always present,
  toxins or physical structures localized at plant
  surface
• Eg.
• 50 angiosperms have secondary compounds at leaf
  surface mixed with wax
• Latex in gt12,000 plant species, viscous white
  fluid, contains rubber particles which act as a
  feeding deterrent terpenoid toxins

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Plant defense mechanisms (cont)

• 2. Induced defenses
• Defenses produced only in response to herbivore
  attack, include both physical and chemical
  defenses
• Plants put off defense until needed -may be
  cheaper, example of adaptive phenotypic
  plasticity

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• Example 1 Increased synthesis of toxins
• May be short term, disappear after insect has
  stopped feeding or may persist over whole season
  or into next year
• Caterpillar larvae feeding on Nicotiana
  sylvestris
• induce 220 increase in alkaloids
• (nicotine nicotinamine) over
• next 5-10 days
• Alkaloids synthesized in roots,
• transported to leaves
• If veins damaged, alkaloid production
• can increase up to 400

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• Example 2 De-novo synthesis of proteinase
  inhibitors
• Colorado beetle feeding on potato or tomato
  leaves
• Proteinase inhibitor inducing factor (PIIF) is
  released into vascular system
• Inhibitor has an adverse effect on the insects
  ability to digest and use plant proteins
• Beetle stops feeding

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• Example 3 Release of predator-attracting
  volatiles
• Cucumbers attacked by spider mite Tetranychus
  urticae release compounds that attract the
  predatory mite Phytoseiulus persimilis

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Herbivore responses to plant defenses

• Herbivores must continually adapt to the
  barriers imposed by their host plants
• No physical or chemical defense is absolute
• 1. Behavioural defenses - herbivores avoid parts
  of plant that are defended
• Eg. Monarch butterfly caterpillars
• feed on latex-producing milkweeds
• Larvae cut the leaf veins before
• feeding, releases latex as a series of
• white blobs along the veins, larvae
• eat between the veins to avoid the
• latex

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2. Sequestration of plant toxins

• Widespread phenomenon, especially in herbivorous
  insects
• Many species that use this technique are
  aposematic (see Lecture18)
• Examples
• Monarch butterflies (see Lecture 18)
• Arctiid moth Utetheisa ornatrix larvae sequester
  pyrrolizidine alkaloids from their host palats,
  toxins retained by adults and passed on by
  females to their eggs. Male transfers unusually
  large spermatophore during mating containing
  nutrients plus alkaloids as a nuptial gift,
• correlated with male size.
• Females select larger males
• and so may reduce the risk
• of predation of their
• offspring

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• 3. Detoxification
• Herbivore uses enzymes to convert toxins to less
  toxic forms
• Often microbial symbionts do the converting
• Many plant toxins are hydrophobic ie do not
  dissolve in water. Detoxification involves
  converting them to more water-soluble substances
  that are more readily eliminated.
• Cytochrome P450s - enzymes used by many
  herbivores in first phase of detox
• Detoxification systems costly --gt most
  herbivores are only adapted to feeding on a few
  species of related plants
• 4. Conjugation
• Herbivore produces a compound that binds to the
  toxin and renders it less harmful
• Eg. gut glycines in lepidoptera act to counter
  the effect of plant tannins (that normally act as
  defensive compounds by binding protein and
  therefore interfere with digestion)

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Herbivore specialization

• Long debated question Why are most herbivores so
  specialized?
• Eg. Dan Janzen collected gt60,000 species of
  Lepidoptera from 725 plant species in Costa Rica,
  gt half the species fed exclusively on one plant
  species, many others fed on only a few species
• This is a general phenomenon ie most insect
  herbivores are oligophagous (feed on a few
  species of related plants)
• Disadvantage
• If host plant unavailable,
• herbivore risks starvation
• (extinction in extreme case)

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• 3 main arguments for the existence of
  specialization

(i) Jack of all trades and master of none
specialists are better at finding and extracting
resources from their hosts than generalists,
selection has fine-tuned physiological and
behavioural mechanisms for maximal efficiency.
Related idea is that the limited neural ability
of insects to process information means that
specialists may be better at finding and using
hosts
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• 3 main arguments for the existence of
  specialization

(i) Jack of all trades and master of none
specialists are better at finding and extracting
resources form their hosts than generalists,
selection has fine-tuned physiological and
behavioural mechanisms for maximal efficiency.
Related idea is that the limited neural ability
of insects to process information means that
specialists may be better at finding and using
hosts
(ii) Value of some plants as hosts lies in their
ability to provide enemy-free space, rather
than just nutritional quality (may explain why
some insects are found on only a subset of plants
on which they are capable of feeding)
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• 3 main arguments for the existence of
  specialization

(i) Jack of all trades and master of none
specialists are better at finding and extracting
resources form their hosts than generalists,
selection has fine-tuned physiological and
behavioural mechanisms for maximal efficiency.
Related idea is that the limited neural ability
of insects to process information means that
specialists may be better at finding and using
hosts
(ii) Value of some plants as hosts lies in their
ability to provide enemy-free space, rather
than just nutritional quality (may explain why
some insects are found on only a subset of plants
on which they are capable of feeding)
(iii) Specialization is not an adaptive trait but
an evolutionary dead end ie direction of
selection in many herbivore groups is toward
increasing specialization until its too late
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Herbivore diversification

• Orders of primarily herbivorous insects are rich
  in species, contribute disproportionately to
  global biodiversity
• Study by Mitter et al (1998) Comparison of 13
  sister taxa where one member of each pair was
  mainly herbivorous and the other non-herbivorous
  showed
• 11/13 pairs showed the herbivorous taxa to have
  at least twice the number of species as the
  non-herbivorous partner
• ie the herbivorous way of life has resulted in
  evolutionary specialization and diversification

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Returning to coevolution

• Coevolution reciprocal adaptation
• Defence and counter-defence of plants and their
  insect herbivores thought to underlie diversity
  of both plant and insect species
• Idea first put forward by Ehrlich Raven
• (1964) noticed that phylogenetically
• related butterflies tended to feed on
• phylogenetically related host plants

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• Hypothetical sequence of events
• Unique genetic event (mutation or recombination)
  occurs in a plant species, confers resistance to
  all or most of its herbivores
• Released from herbivory, plant is able to occupy
  new adaptive zones and radiate
• Insect species experiences unique genetic event
  that confers upon it the ability to overcome the
  novel plant defence
• Released from competitors, the insect undergoes
  adaptive radiation and eventually, derived
  species will use many if not all of the plant
  species
• and so on

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Resulting phylogenies
1
1
2
2
3
3
4
4
5
5
Herbivore species
Plant species
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• Problems with reciprocal coevolution concept
• Difficult to test (cannot directly observe these
  evolutionary events because they occur over very
  long time)

• More evidence that secondary chemicals affect
  herbivores than the other way around
• ie relationship often seems very asymmetric and
  the classic co-evolutionary type hypothesis may
  simply not be appropriate in most cases.

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Alternative view Sequential evolution

• Evolution of flowering plants largely driven by
  factors like climate and soil resources (rather
  than insect attack). This has created a
  chemically diverse trophic base for the evolution
  of herbivores.
• Central idea is that plants loom large in the
  lives of herbivores, but not vice versa.

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Ecological impacts of herbivory

• Tissue removal by herbivores generally reduces
  plant fitness (although many plants produce
  compensatory growth)
• Herbivores remove an average of 18 terrestrial
  plant biomass and 51 aquatic biomass
• Study by Morrow LaMarche (1978) sprayed
  eucalypts with insecticide for several years,
  after 3 yrs sprayed trees were 100 taller than
  unsprayed trees

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Ecological impacts of herbivory (cont)

• Herbivores may also affect plants by being
  disease vectors
• Eg Dutch elm disease struck North American
  forests in 1930s, removed elm as canopy
  dominants, caused by fungus Ceratocystis ulmi,
  carried by elm-bark beetle

• At least 380 plant viruses known to be vectored
  by insects, particularly aphids, but also thrips,
  beetles and mites
• Some insects so effective they are used in
  biological control programs to carry pathogens of
  pests

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Ecological impacts of herbivory (cont)

• Interference with pollination
• Leaf and floral damage can affect attractiveness
  of plants to pollinators
• Herbivore damaged plants may therefore become
  pollen limited

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Herbivore control of plant populations

• Opuntia stricta introduced in mid 1800s as an
  ornamental plant, turn of century escaped
  covered 20 million ha by 1920, 24 million by
  1930.
• Female Cactoblastis cactorum lay eggs on the
  cactus pads, caterpillars eat the cactus from the
  
• inside of the pad, also introduce
• bacteria and fungi as they burrow.
• Moth was very effective as a
• biological control agent because it
• also served as an effective
• vector of pathogens

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• Populations of Opuntia collapsed after release of
  moth, took only 2 yrs to reduce density from
  12,000 indiv per ha to 27. Area covered fell to
  few thousand ha
• Cactoblastis - not complete eradication , cactus
  manages to disperse to moth-free areas, thereby
  keeping one step ahead of the moth, maintains low
  level equilibrium in a continually shifting
  mosaic of isolated patches. Moths also at low
  population levels

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Conclusions

• Herbivory plays a fundamental role in ecosystems
• Herbivores can have important impacts on the
  populations of their host plants
• Plants present formidable obstacles (both
  physical chemical) to insect herbivores
• The few orders of insects that have adapted to
  feeding on plants have undergone a vast
  radiation, presumably as a result of an
  evolutionary arms race
• As a result, green plants and their insect
  herbivores comprise a substantial component of
  global biodiversity