Parasitoids

1. Parasitoids Peter B. McEvoy Ent 420/520 Insect Ecology

2. Parasitoids Cynipoidea: Eucoilidae Ichneumonoidea: Ichneumonidae Proctotrupoidea: Roproniidae Chalcidoidea: Torymidae Diptera: Tachinidae Godfray 1994

3. Parasites Among British Insects

4. 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.

5. 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

6. 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

7. 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).

8. 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?

9. Basic Model Nt+1 = Nt g(Nt) f(Nt,Pt) Pt+1 = c s Nt [1 - f (Nt,Pt)] • Nt, Nt+1, and Pt, and Pt+1represent 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.

10. 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.

11. 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)

12. 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 steadyif parasitism sufficiently clumped. “CV2 >1 rule” or Coefficient of Variation (CV2= variance/mean2) of the density of searching parasitoids in the vicinity of each host exceeds ~1

13. Patterns of parasitism in relation to host density Parasitism may be directly density dependent (DD), inversely density-dependent, or independent of host density CV2=1.52 CV2=0.37 CV2=0.34 CV2=7.33 CV2=0.05 Hassell and Godfray 1992

14. 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

15. Aphytis and Red ScaleA test of parasitoid-host theory • Interaction between red scale Aonidiellaaurantii, 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)

16. Model of Life Cycle

17. Temporal Variation in Parasitism over 28 months

18. 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.

19. 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

20. 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.

21. A Refuge for Red Scale at Interior of Tree

22. History of Competitive Displacement in Aphytis Parasitoids • Aphytis chrysomphali • A. lingnanensis • A. melinus Displaced by Displaced by

23. Mechanism of Competitive Displacement in Aphytis Minimum host size required for female progeny is larger for inferior competitorA. lingnanesis (right arrow) than for superior competitor A. melinus (left arrow)

24. 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 differentiationfor parasitoids attacking the same stage (cocoon)

25. 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.

26. Evidence of Foraging SpecializationWing area in relation to host stage (dispersion) in females

27. 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)

28. Relationship Between Fecundity and Ovariole Number in Ichneumonidae Allows us to use ovariole number as an easily measured index of fecundity

29. Evidence of Reproductive SpecializationReproductive capacity in parasitoid related to probability of survival of host (and parasitoid within)

30. Ovariole Number Inversely Related to Survival Probability Egg Production Survival Probability Balanced mortality hypothesis: egg production adapted to counter the risk of mortality

31. Ovariole number of many Ichneumonidae declines with advance in Host Stage Attacked Gregarious as larvae Attacks egg clusters

32. Females of 4 Species of Parasitoids Attacking Cocoon Stage of Swaine Jack Pine Sawfly Note differences in wing area and ovipositor length

33. Niche Separation Along a Resource Axis

34. Ratios in Ovipositor Lengths in Parasitoids Attacking Sawfly Pupae: Too Close for Coexistence?

35. Response of Parasitoid Species to Increasing Host Density

36. 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 !

37. Dynamics in SpaceRelative Abundance of Cocoon and Larval Parasitoids From Center (Heavy Damage) to Edge (Light Damage) of Outbreak

38. 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.

39. Diffusion theory: Mobile Parasitoids May Restrict Spatial Spread of an Insect Outbreak

40. 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

41. Cast of Characters Herbivore:Orgyia vetusta (Lymantriidae) Plant:Lupinus arboreus and L. chamissonis

42. 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