Migration

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

2. Objectives • Measure and model migratory movement in relation to habitat persistence • Distinguish migration from other forms of movement • Place movement in context of life histories • Identify physiological controls • Appreciate role of Mathematical Theory • Discuss causes and consequences of polymorphism in migratory capacity • Illustrate role of migration in pest outbreaks • Illustrate role of movement and spatial heterogeneity in Population Dynamics

3. Importance of Migration to Many Fields • Ecology – changes in population size, founding of new populations, outcome of species interactions • Behavior-movement a process involving decisions such as when to move, what direction to take, and when to stop • Physiology – environmental variables that induce migration (photoperiod, population density, food quality, and weather patterns) and neural and hormonal mechanisms that process those cues • Evolutionary Biology-an adaptation correlated with spatial and temporal patterns of habitat suitability • Population Genetics – genetic differences in tendency to move may constitute polymorphism; movement often results in gene flow, and gene flow may counteract tendency toward local genetic differentiation • Applied Entomology – techniques for measuring, predicting, controlling movement

4. Migrant Pests Potato leaf hopper Empoasca fabae Six-spotted leafhopper Macrosteles fascifrons (HOMOPTERA: CICADELLIDAE) Arrive suddenly, often in vast numbers, in northern regions where breeding is not active. Apparently migrate in spring from lower Mississippi Valley breeding grounds, aided by southerly winds.

5. Painted LadyVanessa cardui Migrations originate in the deserts of Mexico, where heavy winter rains trigger growth of larval food plants. Photos by Mario Maier

6. Persistent Unanswered Questionsabout Migrants • What proportion of northern populations accounted for by immigration vs. local breeding? • Does a return southward migration occur in the fall? • What are the distances travelled by individual migrants? • Is northward spread achieved by a single generation or by series of northward advances by separate generations?

7. U Fla book of records: Longest Migration. desert locust, Schistocerca gregaria(Acrididae) migrated westward across the Atlantic ocean 4500 km during the fall of 1988

8. Importance of Migration to Ecology • Habitat.Essential in temporary habitats, retained in persistent habitats • Stability. Can stabilize population fluctuations and species interactions • Gene flow.Determines gene flow and genetic structure of populations • Resource allocation and life cycle.Migration a costly part of total resource allocation – resource limitation may require a trade-off between migration and reproduction

9. Evolving Dispersal Weighing benefits and costs Trends in Ecology and Evolution, 2000, 15:1:5-7

10. Literature on wing polymorphism and migration • Southwood 1962 • JS Kennedy • Johnson 1969 • Dingle 1972, 1985 • Harrison 1980, Hardie and Lees 1985, Pener 1985, Roff 1986 • Zera and Denno 1997 Ann Rev Entomol 42:207-231

11. Distinguishing Features of Migration as a form of Movement • Persistent • Straightened-out track • Undistracted by resources that would ordinarily halt it • Distinct departing and arriving behaviors • Energy is reallocated to sustain it

12. Example of active dispersalGreat Southern White Butterfly(Ascia monuste: Pieridae ) • Strong control over flight within the boundary layer

13. More nearly passive dispersal Black Bean Aphid (Aphis fabae) • Passive dispersal: flies above boundary layer where its air speed swamped by wind speed • Element of active control in entry, maintenance, and exit • Life cycle includes alternation between winged and wingless forms Alate or winged Aptera or wingless • Alate formation can be suppressed by increasing temperature, increased by crowding, suppressed by ant attendance, increased by enemies

14. Cabbage Aphid Brevicoryne brassicae(Homoptera: Aphididae) Population begins with a small proportion of alatae at low population densities, and the proportion increases as population grows. Not reversible, but instead local colony eventually disappears

15. Spring and Fall Migration of the Monarch Butterfly

16. Relationship Between Dispersal and Life History Parameters (Dingle 1972)Outline of Study • Individual should have high ‘reproductive value’ when it migrates • Mechanisms that enforce delay in reproduction until after migration (photoperiod) • Effect of environment and selection on flight tendency (temperature, diet, photoperiod, genetics) • Population growth potential of migrant and post-migrant

17. Concept Alert! • Natural selection – differential change in relative frequency of genotypes due to differences in the ability of their phenotypes to obtain representation in the next generation • Heritability – the fraction of variance in a given characteristic of a population that is due to genetic variation in the population • Fitness – the relative rate by which the frequency of a given genotype is increased each generation by selection

18. Concept Alert! • r the intrinsic rate of increase; the fraction by which a population changes in size in each unit of time • R the net reproductive rate; the average number of females produced in the next generation by each female in the present generation •  = lnr = the finite rate of increase; the fraction by which a population changes in size in each unit of time

19. Concept Alert! • vxreproductive value – the expected number of offspring contributed to future population growth by female of age (or stage) x

20. Tropical genus of milkweed bugs Range of 1 sp in genus, O. fasciatus, extends into temperate zone Reproduces on developing pods Short days (12:12 LD) trigger migration southward A Migrant Milkweed Bug    Oncopeltus fasciatus(Lygaeidae)

21. Nonmigrant relativeSmall Milkweed Bug Lygaeus kalmii

22. Table 1. Effect of environment (temperature, starvation, photoperiod) and selection on fight in milkweed bug Oncopeltus fasciatus • Contrast 1 and 3 Effect of temperature • 1 and 5 Effect of starvation • 1 and 4 Effect of photoperiod • 1 and 2 Effect of selection Dingle 1972

23. Table 2. Effect of day length, temperature on intrinsic rate of increase in Oncopeltus fasciatus • Compare 1 and 2 Effect of Photoperiod • 3 and 4 Effect of Photoperiod • 1 and 3 Effect of Temperature • 2 and 4 Effect of Temperature Dingle 1972

24. Gadgil’s TheoryMathematical Theories of Dispersal • Conceptualizes an array of habitat patches which vary in carrying capacity ki(t) • Examines influence of variation in the k's on magnitude of dispersal and sensitivity to crowding • When k's constant or k's vary in phase, selection will favor a low magnitude of dispersal, but higher sensitivity to crowding • When k's vary out of phase, selection favors increasing magnitude of dispersal and decreasing sensitivity of density response

25. Empirical Patterns: Relation between flight ability and habitat in water beetles in England How reliable are inferences from observational data?

26. Dispersal Polymorphism in Insects • Taxonomic Occurrence in insect orders (next slide) • Importance for understanding population dynamics and species interactions, life history evolution,and physiological basis of adaptation • Temporal Hypothesis. Habitat persistence selects for reduced dispersal capability (Denno) • Spatial Hypothesis. Habitat continuity/isolation selects for reduced dispersal capability (Dixon) • Constraints. Fitness trade-off between dispersal and reproduction results from trade-off in allocation of internal resources

27. Orthoptera Psocoptera Thysanoptera Homoptera Heteroptera Coleoptera Diptera Lepidoptera Hymenoptera Taxonomic distribution and types of dispersal polymorphism • Forms of dispersal polymorphism • Wing polymorphism • Flight muscle polymorphism

28. Dispersal capability of wing forms • Migrants. Long-winged form (“macropter”) only form capable of flight, primarily responsible for escaping deteriorating habitats and colonizing new ones • Genetics, environment. Wing morph can result from genetic, environmental, or genetic x environmental variation • Genetics. Polygenic control more common in Orthoptera, Demaptera, Homoptera, Heteroptera; single-gene control in Coleoptera and Hymenoptera.

29. Life History Evolution • Traits: migration, diapause, age at first reproduction, fecundity linked in syndrome • Trade offs between dispersal and fitness components for females • Fecundity lower in macropters (grasshoppers, crickets, planthoppers, aphids, waterstriders and veliids, water boatmen, seed bugs, pea weevils) • Reproduction delayed in migratory forms of grasshoppers, crickets, aphids and planthoppers, waterstriders, true bugs, and beetles • Trade off between dispersal and fitness for males – cost of reproduction generally lower in males

30. What behaviors may partially compensate for inherently lower reproduction in macropters? • Selective colonization of nutrient-rich resources • Large body size and correlated fecundity • Trading off small egg size for increased egg number • Histolyis of wing muscles upon arrival in new habitat with energy reallocation to reproduction

31. WHAT DETERMINES WING FORM? • A hormonally controlled developmental switch that responds toenvironmental cues • CROWDING • HOST PLANT CONDITION • TEMPERATURE • PHOTOPERIOD • So, depending on the conditions it experiences as a nymph, an individual will molt into either a brachypter (short-winged) or macropter (long-winged).

32. Physiological Control of Wing Polymorphism • Hormones. Endocrine regulation of morph development based on level of JH and ecdysone shown for the case of one cricket species • Environmental cues such as crowding, host plant condition, temperature, and photoperiod influence wing form • Sensitive stage can occur prenatal, postnatal, middle (e.g. planthoppers), late stages (e.g. crickets)

33. PLANTHOPPERSDELPHACIDAE Macropter Brachypter Study system provides the first rigorous assessments of the relationship between dispersal and habitat persistence

34. Migration in Relation to Habitatfor the salt marsh planthopper Prokelisia marginata • Emerge winter-spring high marsh • Migrate spring-summer to low marsh • Thrive in Summer low marsh • Return migration in Fall to high marsh

35. Fig 1. Macroptery decreases as habitat persistence increases for 35 spp planthoppers Test of hypothesis requires operational definitions of variables: dispersal capability and habitat persistence Females Males Relationship is nonlinear

36. Negative relation between dispersal and habitat persistenceSummary of Evidence • Interspecific contrasts. For 35 species of planthoppers inhabiting low-profile vegetation, there was a significant, negative, nonlinear relationship between dispersal capability (% macroptery) and the persistence of their habitats (maximum number of generations attainable) • Phylogenetically-independent contrasts. Same result for phylogenetically independent contrasts between congeners • Intraspecific contrasts. Negative relationship between dispersal capability and habitat persistence found • True for ‘2-D habitats’, but not for ‘3-D habitats’, e.g. wing polymorphic and flightless species tend to be rare in trees

37. Fig 2. Effect of Crowding: Macroptery increases with rearing density for Prokelisia marginata and P. dolus P. marginata Temporary habitat Highly migratory Males > Females P. dolus Persistent habitat Less migratory Males ~ Females Summary of Effects Species: Differences between species Gender: Differences between male and female with species Gender x Species:Gender difference varies by species

38. Fig 3. Macroptery Response to Rearing Density for 5 Other planthoppers All species are migratory and occur in temporary habitats except M. fairmairei, which resides in persistent grasslands • Varies by • Species • Gender - • Gender x Species

39. Genetic variation within a single species?% macroptery reponse to rearing density for P. marginata from (A) temporary (NJ) and (B) persistent (FLA) habitats What constitutes appropriate and adequate replication in this comparison? Temporary (NJ) Persistent (FLA)

40. Male Bias in macroptery found in habitats of low persistenceMales are more likely than females to remain in temporary habitats Null expectation males/females

41. Gender differences • Macroptery increases with local density: Females often more sensitive to increasing density than males. Why? • Cost of reproduction higher in females than males. Why? • Trade off between reproduction and dispersal well documented in females. How? • Similar trade off can occur in males. How? • Dual role of wings in colonization and mate location. In temporary habitats, wings may be retained in males to locate females at low colonizing densities. How might we separate contributions of migration to mating and colonizing ability?

42. Conclusions • Separating influences of environment and ancestry: Habitat persistence has influenced migration independently of common ancestry • Interactions of factors: Habitat persistence also influences the wing-form response of planthoppers to crowding. • Flight reflects multiple selective forces; Density wing-form responses of planthoppers reflect two density-related advantages of flight: Habitat escape and Mate location.

43. Summary and Future Directions NOW We have rigorous assessments of • Relationship between habitat stability and dispersal capability • Trade-off between flight capability and reproduction (including physiological basis) • Endocrine control of flight capacity in a wing-dimorphic insect (cricket) FUTURE We need further investigation of • Trade-off between flight capacity and reproduction in males • Endocrine control known only for one species • Ecological and physiological mechanisms in same species • Fates of migrants and nonmigrants, reliability of wing polymorphism as index of migration • Migration in the context of population dynamics at landscape scale

44. Migration in the Context of Population Dynamics • Several species of forest insects exhibit outbreaks • Progress being made on temporal patterns and underlying mechanisms (Turchin 1990; Berryman 1996) • Outbreaks can also exhibit a sptio-temporal pattern known as ‘traveling waves’ (Johnson, Bjornstad, Liebhold 2004 Ecol Letters 7:967-974)

45. Landscape Ecology in a Nutshell • The field of landscape ecology addresses how landscape mosaics -- i.e. the spatial interspersion of favorable habitats ('patches') and non-favorable habitats ('matrix) - affect ecological processes (Turner et al. 1989, Wiens et al. 1993). • The idea is that the proximity of favorable habitats, and/or ‘permeability’ (Stamps et al. 1987) of any matrix habitat, will enhance the exchange of migrants (‘connectivity’) between such habitats. Thus persistence of sink populations can be enhanced by subsidies from source habitats, the growth of satellite populations fueled by waves of immigrants. • Previous studies suggest that landscape heterogeneity and fragmentation can affect the dynamics of pest populations (Shigesada et al. 1986, Roland 1993).

46. Herbivore population dynamics:larch budmoth in Swiss Alps(Zeiraphera diniana Gn.) • Remarkably regular 8-10 yr cycle • Covering 5 orders of magnitude per cycle O.N. Bjørnstad, M. Peltonen, A. M. Liebhold, W. Baltensweiler2002 Science 298:1020-1023.

47. Time series of larch budmoth larval density (average of 5 permanent sites) and defoliation (all Alps). Damage can be used as a surrogate for insect density Phase: 8-9 yr cycle Amplitidue: 5 log-cycles This figure shows that defoliation time-series very closely tracks time-series in actual population density and thus serves as an adequate proxy to population density

48. Trophic hypotheses for Larch BudwormTop-Down or Bottom-Up or Other? • Food quality – defoliation low quality needles (higher fiber, lower N) reduced larval survival and female fecundity • Pathogens – granulosis virus • Parasitoids – parasitism rates low (10-20%) at peak LBM to high (90%) 2-3 yr after peak • Polymorphic Fitness hypothesis – dark morph (deciduous larch) increases during population increase and light morph (evergreens) increases during population collapse • Other hypotheses – host quantity, predators Turchin concludes plant quality and parasitism interact in their effects (Turchin)

49. Color pattern varies during the cycle Are evolutionary changes in budworm population contributing to cycles in dynamics? • Dark vs Light. The larch form caterpillars are usually dark, but during the decline phase, lighter forms appear. • Selection vs gene flow. May reflect gene flow from the pine form of the moth, or selection within the larch form population • Cause vs consequence. Changes in morph frequency may be a consequence of changes in density, rather than a cause of changes in density

50. Mortality L3 (%) Pupal mass (mg) Leaf fiber content (%) Are changes in host quality (leaf fiber content) contributing to budworm dynamics?Plant Quality and Larch Bud Moth Performance Larval mortality increases with fiber content of needles Pupal mass decreases with fiber content of needles