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
Photos by Mario Maier

• Migrations originate in the deserts of Mexico,
  where heavy winter rains trigger growth of larval
  food plants.

6
Persistent Unanswered Questionsabout Migrants

1. What proportion of northern populations accounted
   for by immigration vs. local breeding?
2. Does a return southward migration occur in the
   fall?
3. What are the distances travelled by individual
   migrants?
4. 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, 1515-7
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 42207-231

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Distinguishing Features of Migration as a form of
Movement

1. Persistent
2. Straightened-out track
3. Undistracted by resources that would ordinarily
   halt it
4. Distinct departing and arriving behaviors
5. 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
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Relationship Between Dispersal and Life History
Parameters (Dingle 1972)Outline of Study

1. Individual should have high reproductive value
   when it migrates
2. Mechanisms that enforce delay in reproduction
   until after migration (photoperiod)
3. Effect of environment and selection on flight
   tendency (temperature, diet, photoperiod,
   genetics)
4. Population growth potential of migrant and
   post-migrant

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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
• ? ln r the finite rate of increase the
  fraction by which a population changes in size in
  each unit of time

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Concept Alert!

• vx reproductive value the expected number of
  offspring contributed to future population growth
  by female of age (or stage) x

20
A Migrant Milkweed Bug    Oncopeltus
fasciatus(Lygaeidae)

• Tropical genus of milkweed bugs
• Range of 1 sp in genus, O. fasciatus, extends
  into temperate zone
• Reproduces on developing pods
• Short days (1212 LD) trigger migration southward

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Nonmigrant relativeSmall Milkweed Bug Lygaeus
kalmii
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Table 1. Effect of environment (temperature,
starvation, photoperiod) and selection on fight
in milkweed bug Oncopeltus fasciatus
Conditions Conditions Sample size Number flying gt30 min Percent flying
(1) 168 LD 23oC Parent 311 74 23.8
(2) 168 LD 23oC Offspring 47 30 63.8
(3) 168 LD 27oC 98 10 10.2
(4) 1212 LD 24oC 54 38 70.4
(5) LD 168 LD Starved 3 days 23oC 148 70 47.3
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
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Table 2. Effect of day length, temperature on
intrinsic rate of increase in Oncopeltus
fasciatus
Conditions Conditions Age 1st reproduction Increase per day r Doubling Time
(1) 168 LD 27oC 47 0.0810 8.90
(2) 1212 LD 27oC Migrant 61 0.0593 12.03
(3) 168 LD 23oC 63 0.0499 14.24
(4) 1212 LD 23oC Migrant 95 0.0369 19.13
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
Gadgils 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

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Empirical Patterns Relation between flight
ability and habitat in water beetles in England
Permanent Temporary Permanent Temporary Permanent Temporary Permanent Temporary Permanent Temporary
Southwood 1962 Rivers springs Lakes, tarns, canals Brackish water, peat bogs Ponds, ditches Artificial ponds, gravel pits, cattle troughs
Able to fly 3 10 30 27 24
Variable 6 13 14 15 8
Unable to fly 13 7 7 2 0
How reliable are inferences from observational
data?
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Dispersal Polymorphism in Insects

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

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Taxonomic distribution and types of dispersal
polymorphism

• Orthoptera
• Psocoptera
• Thysanoptera
• Homoptera
• Heteroptera

• Coleoptera
• Diptera
• Lepidoptera
• Hymenoptera

Forms of dispersal polymorphism Wing
polymorphism Flight muscle polymorphism
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Dispersal capability of wing forms

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

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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

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What behaviors may partially compensate for
inherently lower reproduction in macropters?

1. Selective colonization of nutrient-rich resources
2. Large body size and correlated fecundity
3. Trading off small egg size for increased egg
   number
4. Histolyis of wing muscles upon arrival in new
   habitat with energy reallocation to reproduction

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WHAT DETERMINES WING FORM?

• A hormonally controlled developmental switch
  that responds to environmental 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

1. Hormones. Endocrine regulation of morph
   development based on level of JH and ecdysone
   shown for the case of one cricket species
2. Environmental cues such as crowding, host plant
   condition, temperature, and photoperiod influence
   wing form
3. 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

1. Emerge winter-spring high marsh
2. Migrate spring-summer to low marsh
3. Thrive in Summer low marsh
4. 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

1. 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)
2. Phylogenetically-independent contrasts. Same
   result for phylogenetically independent contrasts
   between congeners
3. Intraspecific contrasts. Negative relationship
   between dispersal capability and habitat
   persistence found
4. 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 gt 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

1. Macroptery increases with local density Females
   often more sensitive to increasing density than
   males. Why?
2. Cost of reproduction higher in females than
   males. Why?
3. Trade off between reproduction and dispersal well
   documented in females. How?
4. Similar trade off can occur in males. How?
5. 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

1. Several species of forest insects exhibit
   outbreaks
2. Progress being made on temporal patterns and
   underlying mechanisms (Turchin 1990 Berryman
   1996)
3. Outbreaks can also exhibit a sptio-temporal
   pattern known as traveling waves (Johnson,
   Bjornstad, Liebhold 2004 Ecol Letters 7967-974)

45
Landscape Ecology in a Nutshell

1. 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).
2. 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.
3. Previous studies suggest that landscape
   heterogeneity and fragmentation can affect the
   dynamics of pest populations (Shigesada et al.
   1986, Roland 1993).

46
Herbivore population dynamicslarch 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.
  Baltensweiler 2002 Science 2981020-1023.

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?

1. Dark vs Light. The larch form caterpillars are
   usually dark, but during the decline phase,
   lighter forms appear.
2. Selection vs gene flow. May reflect gene flow
   from the pine form of the moth, or selection
   within the larch form population
3. Cause vs consequence. Changes in morph frequency
   may be a consequence of changes in density,
   rather than a cause of changes in density

50
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
51
Larch Budmtoh Zeiraphera diniana in European
AlpsSpatio-Temporal Pattern of Dynamics
Wave travels from 219.8 to 254 km/yr in NE direct
(varying with method of estimation)

• http//www.sandyliebhold.com/pubs/science_DC1/

52
Epicenter Hypothesis

1. Regional outbreaks begin in specific foci and
   then spread into adjoining areas
2. Example include spruce budworm, gypsy moth, and
   mountain pine beetle
3. Commonly claimed that outbreak starts in habitats
   of high quality (i.e. where population growth
   rate is highest) and spread via dispersal to
   elevate pest densities in surrounding suboptimal
   habitats to initiate secondary outbreaks
4. There is evidence contradicting this
   hypothesisforcing a modification of the
   epicenter hypothesis

53
Spatial Version of Nicholson-Bailey Model
Capatures nonlinear parasitoid-host interaction

1. Spatially-distributed population models predict
   complex spatial dynamics, such as spiral waves
   and spatial chaos, as a result of trophic
   interactions
2. Bjornstad et al (2002) demonstrate the existence
   of waves in Central European larch budmoth
   (Zeiraphera diniana Gn.) outbreaks
3. Waves travel toward the northeast-east at 210 km
   per year later revised to 254 km per year
4. A theoretical model involving a moth-enemy
   interaction predicts directional waves, but only
   if dispersal is directionally biased or habitat
   productivity varies across the landscape. Later
   revised to emphasize habitat geometry and
   dispersal.
5. Study confirms that nonlinear ecological
   interactions can lead to complex spatial dynamics
   at a regional scale

54
Nicholson-Bailey Type Models

• Discrete-time models designed mainly for annual
  insects with one generation per year and no
  overlap in generations.
• 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
• f(Nt,Pt) gives host survival with respect to
  parasitoid and host densities and can be varied
  to reflect variation in parasitoid foraging
  behavior

55
Outbreaks originate (left) in areas of high
connectivity (right)
56
Vector Plot showing local relative speeds and
directions

• Vector plot indicating local relative speeds and
  directions of larch budmoth wave movement across
  the Alps. The circles indicate two-wave
  epicentres.

57
Summary LBM Study

1. Travelling waves in cycling populations highlight
   the importance of migration in population
   dynamics
2. Waves in LBM outbreaks originate from two
   epicenters, both located in high concentrations
   of favorable habitat
3. Movement in relation to ecosystem texture may be
   responsible for travelling waves
4. A tri-trophic model of LBM show landscape
   heterogeneity (specifically gradients in density
   of favorable habitat) sufficient to induce waves
   from epicenters