Parasitoids

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Parasitoids

• Peter B. McEvoy
• Ent 420/520 Insect Ecology

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Parasitoids
Cynipoidea Eucoilidae
Ichneumonoidea Ichneumonidae
Proctotrupoidea Roproniidae
Chalcidoidea Torymidae
Diptera Tachinidae
Godfray 1994
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Parasites Among British Insects
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Parasitoid Natural History(Godfray 1994, Quicke
1997)

• Endoparasitoids feed and develop within the body
  of the host ectoparasitoids live externally,
  normally with their mouthparts buried in the body
  of their host.
• Solitary parasitoids develop singly on or in
  their hosts gregarious parasitoids develop in
  groups ranging from two to several thousand
  individuals feeding together on a single host.
• Superparasitism occurs when single parasitoid
  species lays more eggs on a single host than can
  be supported by that host mutiple parasitism
  occurs when more than one parasitoid species
  parasitizes the same host.
• Hyperparasitism occurs when a secondary parasite
  parasitizes a primary parasite. Facultative
  hyperparasites can develop on unparasitized host
  individuals and only develop as hyperparsitoids
  when eggs are laid on a previously parasitized
  host obligate hyperparasitoids are only able to
  develop as parasitoids of parasitoids.
• Parasitoids that allow hosts to continue to grow
  in size after parasitism are call koinobionts as
  opposed to idiobionts, where the parasitoid
  larvae must make do with the resource present at
  oviposition.

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Importance of parasitoids in population dynamics
of their hostsFour Lines of Evidence

• Mathematical models. Theoretical studies of
  host-parasitoid dynamics
• Laboratory. Laboratory experiments showing
  suppression and persistence under controlled
  conditions
• Biological control. Success of some biocontrol
  programs indicates strong suppression and
  persistence at low densities
• Pesticide disruption. Pest resurgence after
  disrupting natural enemies with pesticides

Hassell and Godfray 1992
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Field studies of the role of parasitism under
natural conditions

• Inadequate analysis or information. Apparent
  absence of DD from some life table studies may
  arise through inadequate analysis and/or
  insufficient data
• Biased selection of study organisms. Organisms
  selected for long-term study because they are
  consistently abundant are likely to be resource
  limited rather than parasitoid regulated

Hassell and Godfray 1992
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Pitfalls in measuring parasitism rates

• In observational studies, hosts may not be
  sampled with equal probability due to differences
  between parasitized and unparasitized hosts in
  development, behavior, and susceptibility to
  other forms of mortality.
• In experimental studies, placing artificial
  cohorts in the field must take account of
  variation in parasitism rates within a host
  population, e.g. among hosts in different stages
  or distributed at different times (phenological
  variation) and places (between different plants
  species and habitats).

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Key components of parasitoid-host dynamics

• Suppression of host population by parasitoid.
  What determines the degree to which a parasitoid
  population can depress average host population
  levels?
• Stability of host-parasitoid interaction. What
  factors are promoting persistence of the
  interacting populations?

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Basic Model

• Nt1 Nt ? g(Nt) f(Nt,Pt)
• Pt1 c s Nt 1 - f (Nt,Pt)
• Nt, Nt1, and Pt, and Pt1 represent the host and
  parasitoid population densities in successive
  generations, respectively,
• ? is the geometric growth rate of the host
  (which can remain constant or change as a
  function of host density according to density
  dependent function ? g(Nt)),
• c is the number of parasitoids produced for each
  host individual attacked (the "numerical
  response" of the parasitoid),
• s is the proportion of parasitoid progeny that is
  female.
• The function f(Nt,Pt) gives host survival with
  respect to parasitoid and host densities and can
  be varied to reflect variation in parasitoid
  foraging behavior.

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Analysis of Basic Model

• Equilibrium levels depend on the balance between
  the rate of increase of the host ? g (Nt)
  compared with the level of parasitism (1-f) and
  the number of surviving female progeny per host
  attacked (cs), all evaluated at equilibrium
• Stability depends on (1) the degree of
  density-dependence, implicit or explicit, in the
  different terms of the equations, (2) the total
  amount of heterogeneity in the risk of parasitism
  among individual hosts.

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Stability enhanced by density dependence in

• Host rate of increase. Factors other than
  parasitism affecting the host rate of increase ?
  g (Nt). Even at low average density, hosts may
  experience density dependence (at least on a
  local scale) in patchy populations.
• Survival from parasitism. Factors affecting the
  overall searching efficiency of the parasitoid
  and host survival from parasitism (f(Nt, Pt))
• Functional responses (See Mathcad or Populus)
• Mutual interference A key component of lab
  interactions, a possible component of field
  interactions when coupled with aggregative
  behavior. (See Mathcad or Populus)
• Heterogeneity in risk from parasitism due to
  spatial distribution of parasitism from host
  patch to host patch, temporal asynchrony between
  host and parasitoid, or different susceptibility
  of individual hosts to parasitism. (See Mathcad
  or Populus)

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Interpreting patterns of parasitism

• Patterns of parasitism in relation to host
  density. Parasitism may be directly density
  dependent (DD), inversely density-dependent, or
  independent of host density
• Stability - populations remain roughly steady if
  parasitism sufficiently clumped. CV2 gt1 rule
  or Coefficient of Variation (CV2
  variance/mean2) of the density of searching
  parasitoids in the vicinity of each host exceeds
  1

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Patterns of parasitism in relation to host
density Parasitism may be directly density
dependent (DD), inversely density-dependent, or
independent of host density
CV21.52
CV20.37
CV20.34
CV27.33
CV20.05
Hassell and Godfray 1992
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Multispecies Interactions

• Two parasitoid species attacking the same host
  species
• Host, parasitoids and hyperparastioids
• Competing host species sharing the same
  parasitoid species
• Hosts attacked by specialist and generalist
  natural enemies
• Host, parasitoids, and pathogens

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Aphytis and Red ScaleA test of parasitoid-host
theory

• Interaction between red scale Aonidiella
  aurantii, and insect pest of citrus, and Aphytis,
  an introduced insect parasite that control red
  scale in many areas of the world
• Natural History of the organisms (refer to figure
  on life cycle)
• Evidence of stable interactions (refer to figure)

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Model of Life Cycle
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Temporal Variation in Parasitism over 28 months
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Approach

• Analyze the foraging behavior
• Determine the consequences for population
  dynamics using mathematical models
• Test by field experiments whether the models
  correctly describe the underlying processes.

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Hypotheses and Field Tests

• Aggregation by parasitoid to local host density -
  Mechanism absent
• Aggregation independent of local host density -
  Mechanism absent
• Parasitoid sex-ratio density-dependent -
  Mechanism absent
• Temporally density-dependent parasitism (also
  delayed) - Mechanism absent
• Temporally density-dependent host feeding -
  Mechanism absent
• Temporally density dependent predation -
  Mechanism absent
• Spatial refuge from parasitism - Mechanism
  present, not stabilizing
• Metapopulation dynamics - Mechanism absent
• Invulnerable class(es) of hosts - Mechanism
  present

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7. Spatial refuge from parasitism. Mechanism
present, not stabilizing.

• Observational studies comparing interior
  populations on the bark of trunk and internal
  branches and exterior populations on the flush of
  new foliage.
• Parasitism rates higher in exterior. Parasitism
  in interior/parasitism in exterior ? 1/15
• Population sizes higher in interior. Refuge
  subpopulation /exterior subpopulation ? 100.
• Movement rates between refuge and exterior
  subpopulations. Sticky traps wrapped around
  branches used to confirm movement.
• Predict exterior populations stabilized by flow
  of crawlers from interior subpopulation.
• Results of experimental removal of refuge
  contradict prediction. An 18-moth field
  experiment removed the refuge population the
  exterior population does not become temporally
  more variable.
• Conclusion. Refuge present, but not stabilizing.

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A Refuge for Red Scale at Interior of Tree
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History of Competitive Displacement in Aphytis
Parasitoids

• Aphytis chrysomphali
• A. lingnanensis
• A. melinus

Displaced by
Displaced by
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Mechanism of Competitive Displacement in Aphytis
Minimum host size required for female progeny is
larger for inferior competitor A. lingnanesis
(right arrow) than for superior competitor A.
melinus (left arrow)
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Parasitoids of sawflies studied by Price

• Parasitoid guild. 11 hymenopterous parasitoid
  species use the same host, the Swaine jack pine
  sawfly Neodiprion swainei
• Life history features. Differences in stage
  attacked force specialization in mobility (wing
  area) and reproduction (ovariole number)
• Niche and habitat differentiation for parasitoids
  attacking the same stage (cocoon)

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Example of 11 hymenopterous parasitoid species
using the same host, the Swaine jack pine sawfly
Neodiprion swainei(Peter Price)

• Foraging specialization Wing-loading related to
  host dispersion (see Figure 8.4). Greater
  mobility (wing area) in parasitoids exploiting
  mobile stages (larvae).
• Reproductive specialization Reproductive
  capacity inversely related to probability of
  survival of larval stage.
• Morphological specialization How similar can
  species become in morphology and resource
  partitioning and remain sympatric (May 1973)?
  Niche partitioning along one dimension
  ovipositor length.
• Alternative explanations of coexistence
  emphasize dynamics of the guild in space and time.

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Evidence of Foraging SpecializationWing area in
relation to host stage (dispersion) in females
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Ovarioles Per Ovary
(A) Enicospilus americanus, a highly fecund
Ichneumod with short ovipositor and larger
lateral oviducts (C) Trachysphyrus albatorius, an
Ichneumonid with few ovarioles, short lateral
oviducts and a long ovipositor)
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Relationship Between Fecundity and Ovariole
Number in Ichneumonidae
Allows us to use ovariole number as an easily
measured index of fecundity
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Evidence of Reproductive SpecializationReproducti
ve capacity in parasitoid related to probability
of survival of host (and parasitoid within)
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Ovariole Number Inversely Related to Survival
Probability
Egg Production
Survival Probability
Balanced mortality hypothesis egg production
adapted to counter the risk of mortality
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Ovariole number of many Ichneumonidae declines
with advance in Host Stage Attacked
Gregarious as larvae
Attacks egg clusters
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Females of 4 Species of Parasitoids Attacking
Cocoon Stage of Swaine Jack Pine Sawfly
Note differences in wing area and ovipositor
length
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Niche Separation Along a Resource Axis
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Ratios in Ovipositor Lengths in Parasitoids
Attacking Sawfly Pupae Too Close for
Coexistence?
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Response of Parasitoid Species to Increasing Host
Density
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Dynamics in TimeParasitoid Species Diversity in
Relation to Host Density

• Diversity of parasitoids in relation to host
  density depends on whether host population is
  increasing (closed circles) or decreasing (open
  circles)
• Claims of hysteresis in the system rest on a
  single point !

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Dynamics in SpaceRelative Abundance of Cocoon
and Larval Parasitoids From Center (Heavy Damage)
to Edge (Light Damage) of Outbreak
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Lessons learned from sawfly parasitoid study

• Foraging specialization Greater mobility (wing
  area) in parasitoids exploiting mobile stages
  (larvae).
• Reproductive specialization Reproductive
  capacity inversely related to probability of
  survival of larval stage.
• Morphological specialization How similar can
  species become in morphology and resource
  partitioning and remain sympatric (May 1973)?
  Niche partitioning along one dimension
  ovipositor length.
• More work on alternative explanations of
  coexistence emphasize dynamics of the guild in
  space and time.

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Diffusion theory Mobile Parasitoids May Restrict
Spatial Spread of an Insect Outbreak
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Necessary and sufficient conditions

• Predator more mobile than prey
• Predator responds numerically to prey so that
  predator becomes concentrated where prey are most
  abundant
• Prey population growth is positively density
  dependent, so that localized patches of prey tend
  to arise
• Under these conditions, mobile predators
  diffusing outward from areas of high prey density
  create surrounding zones in which predator-prey
  ratios and hence rates of predation are elevated

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Cast of Characters
Herbivore Orgyia vetusta (Lymantriidae) Plant
Lupinus arboreus and L. chamissonis
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Test of Theory (Brodmann et al. 1997)

• Western tussock moth Orgyia vetusta
  (Lymantriidae) outbreaks on shrubby lupine
  (Lupinus arboreus and L. chamissonis) in coastal
  California tend not to spread
• Placed eggs and larvae of host along a 500-m
  transect leading away from the edge of a tussock
  moth outbreak
• Measured attack rates by a wasp egg parasitoid
  and four species of tachinid fly larval-to-pupal
  parasitoids
• As predicted, rates of parasitism were elevated
  in the zone surrounding the outbreak
• Results are consistent with several explanations,
  including the predator diffusion hypothesis
• In any event, parasitism restricts spatial
  distribution of host insect