Herbivore-Plant Interactions 2 : Seed-Slayers

1
Herbivore-Plant Interactions 2 Seed-Slayers

• Peter B. McEvoy
• Oregon State University

2
Outline

• The nature of seed slaying
• Characteristics of seeds
• Taxa engaged in attack seeds
• Species packing among fig bugs
• Impact of seed slayers
• On plant communities
• On plant populations

3
Characteristics of Seeds

• Nutrient values per unit volume high
• Shorter time courses
• Once dispersed, hard to find
• Chemical defense might be greater low self
  repair
• Continuous seed production not required for
  survival of plant except in case of annual
  without a seed bank
• Result Seed timing, quality and quantity can be
  more freely manipulated by natural selection that
  those same characteristics of leaves and other
  vegetative parts

4
Taxa engaged in seed slaying

1. Coleoptera (Curculionidae, Bruchidae)
2. Heteroptera (Lygaeidae, Phyrrhocoridae)
3. Lepidoptera (Pyralidae, Tortricidae,
   Olethreutidae, Lycaenidae)
4. Hymenoptera (Formicidae, Chalcidoidea)
5. Diptera (Tephritidae)
6. Mammals and Birds

5
Seed-Slaying ColeopteraSeed weevils (Bruchidae)
occasionally become pests of stored beans,
cowpeas, and peas
Pea Weevil Bruchus pisorum (Linnaeus)
Acanthoscelides obtectus (Say) Bean weevil
weevil Curculio glandium attacking acorn of
English Oak Quercus robur
6
Seed Slaying Heteroptera (Lygaeidae,
Phyrrhocoridae)
Oncopeltus fasciatus
Lygaeidae Oncopeltus fasciatus feeds on
developing pods of milkweed, requires seeds for
reproduction
Pyrrhocoridae Dysdercus saturelluspest of
cotton, damages developing bolls causing plant
sap to exude from feeding site
7
Seed slaying Lepidoptera Pyralidae
Ostrininia nubilalis
European Corn Borer Ostrinia nubilalis attacks
corn, sorghum, cotton, and many vegetables,
causing damages in US gt 1 billion annually.
Introduced to NA in early 1900s.
8
Spruce budwormChoristoneura fumiferanaTortricida
e
Dispersing larva dangling on a silken thread
One of most destructive native pests of spruce
and fir forests in eastern NA
Sister species, western spruce budworm,
Choristoneura occidentalis, defoliator of
coniferous forests in W NA
Adult and pupa
9
Codling mothCydia pomonella Lep Tortricidae,
Olethreutinae
Multivoltine, destructive pest introduced to NA
by EU settlers. Larvae tunnel into center of
fruit where they feed and develop.
Oriental fruit moth Grapholitha molesta
10
Mexican jumping bean mot Lep Tortricidae Cydia
saltitans

• Mexican jumping bean - seed of Mexican shrubs of
  the genus Sebastiana (Euphorbiaceae) containing
  the larva of a moth whose movements cause the
  bean to jerk or tumble

11
Hymenoptera(Formicidae, Chalcidoidea)
Alfalfa Seed Chalcid  

• seed-harvesting ant species in the genera Messor,
  Pheidole and Pogonomyrmex

Pogonomyrmex (naegelii-group) imberbiculus
AntWeb California Academy of Sciences
12
Diptera Tephritidae

• Above Urophora stylata female and 2 males.
  Imported to NA for BC thistles
• Photos by Albert Krebs

Right Rhagoletis completa breeds in the husks of
walnuts (Juglans spp.). Photo by Erwin Mani
http//www.sel.barc.usda.gov/Diptera/tephriti/Phot
Tour/Photos.htm
13
Mammals and Birds

• Orangutans and parakeets feed on dipterocarp
  seeds. (B) A carpet of dipterocarp seedlings
  established during the 1987 mast-fruiting event.
  (D) Dipterocarp trees in Borneo's Gunung Palung
  National Park. ECOLOGY Tropical Forest Synergies
  by Gary Hartshorn and Nora Bynum

14
Effects of seeds on InsectsLygaeid bugs as seed
predators of figs Ficus spp (Moraceae)

• Arboreal feeders
• Obligate terrestrial
• Early species
• Late species
• Facultative terrestrial
• Predispersal seeds are a concentrated resource
• Mechanisms facilitating exploitation of a patchy
  resource, macroptery and ovoviparity

Slater 1977
15
Fluctuations in abundance of fig foliage
unrelated to herbivores

• Fig leaves added after original fresco was
  painted, probably at the request of Cosimo III
  de' Medici in the late 17th century, who saw
  nudity as disgusting. Leaves were removed when
  painting restored in 1980s

Masaccio The Expulsion Of Adam and Eve from Eden
(1426-28) fresco in Florence
16
Are plant populations seed-limited?

• Turnbull, L. A., M. J. Crawley, and M. Reese.
  2000. Are plant populations seed-limited? A
  review of seed sowing experiments. Oikos
  88225-238.
• Definition. They define seed limitation to be an
  increase in population size following seed
  addition.
• Two types of experiments. They review two types
  of seed addition experiments seed augmentation
  studies where seeds are added to existing
  populations and seed introductions where seeds
  are sown in unoccupied sites.
• Overall results. Approximately 50 of seed
  augmentation experiments show evidence of seed
  limitation. These studies show that seed
  limitation tends to occur more commonly in early
  successional habitats and in early successional
  species.

17
Protocol recommended for seed addition
experimentsmodified from Turnbull et al. 2000

1. Estimate seed output of natural population.
   Facilitate comparison by making seed addition
   some specified multiple of natural seed rain.
2. Manipulate seed outputs over a sufficient range.
3. Monitor response throughout the life cycle, at
   least to adult stage.
4. Manipulate seed-feeding herbivores as part of the
   design. Combine enhanced, control, and diminished
   seed predators with enhanced, control, and
   diminished seed rain.
5. Conduct additions on appropriate spatial and
   temporal scale. Mimic the spatial and temporal
   scale "sampled" by the life history of the
   organism.

18
Seed limitation more common in early successional
habitats
Varies from strong seed-limtation to strong
micro-site limitation
19
Seed limitation more common in early successional
species (confounded with habitat)
20
Impacts of seed predators on thistles studied by
Svata Louda
Rhinocyllus conicus
Svata Louda

• Introduced weevil invaded Nebraska sand dunes
  where Louda was studying native thistles

Thistle in Sand Dune Habitat
21
Effects of Insects on Reproductive Success of
Cirsium canescens

• Removal experiment insecticide
• Herbivore effect protected exposed
• Spatial, temporal, organizational scales of
  observation
• Temporal scales (within and between years)
• Spatial scales (region, habitat, between plant,
  within plant)
• Organizational scales (plant/arthropod
  association, guild, and species within guild
• Platte thistle inflorescence feeders
• Tephritid flies Orellia occidentalis and
  Paracantha culta
• Pyralid moth Hoemosoma stypetallum

22
Life Cycle Graph for Thistle
23
Seedling Shadows with and without insecticide
Seed predator effect conditional on
distance Recruitment declines with distance from
parent Higher recruitment rate when insects are
removed using an insecticide at shorter distances
24
Seed Predator Effects Conditional on Year and
Habitat
25
Lifetime Seed Production higher in Protected vs
Exposed Plants (Louda and Potvin 1984)
26
Plants responses to heavy exploitation by seed
slayers

• Evolving deterrents (may increase confer
  resistance or increase handling time for
  consumer)
• Hard Seed coat
• Toxic chemistry
• Mast cropping escape in time -synchronous, mass
  production of fruits at interval of n years with
  very light crops or no crop in intervening years
• May lead to Predator Satiation producing so
  many seeds that slayer cant use them all
  (saturates consumers functional response)
• Intervals of little or no seed mitigiate risk of
  predator increase (counters consumers numerical
  response)
• Rapid dispersal escape in space

27
Problem for Community Ecologists

• Seeds slayers have been invoked in explanations
  of the extraordinary species richness of tropical
  forests
• For example, how are we account for the more than
  700 species of trees, shrubs and linas (vines)
  found on 17 km2 of Barro Colorado Island, Panama?
• Two aspects of the problem
• Evolutionary question origins of so much
  diversity, so many species
• Ecological question maintenance of diversity,
  what prevents competitive exclusion

28
Janzen-Connell Model

• Seed Shadow (I curve) seed density falls off
  with distance from the parent. Shape varies with
  size of seed crop and model of dispersal.
• Probability of Survival (P curve) increases
  with distance from the parent. Seed slaying
  varies with distance and/or density.
• Population Recruitment Curve (PRC curve) Taking
  the product of the I and P curves yields the
  recruitment curve

29
Janzen-Connell Model
Distance from parent tree

• Dispersal (I), Survivorship (P), Recruitment (PRC)

30
Question

• To what extent can seed predation alone lead to
  variable recruitment patterns?
• Which components of predator activity are
  responsible for this variation?
• How are they responsible?
• Model varies the
• Number of dispersed seeds
• Mean distances of dispersed seeds
• Predators activity

31
Basic Model(Nathan and Casagrandi 2004 J Ecol)

• Dynamics of seeds S at distance ? from the source
  over time t reflects balance in seed gains (the
  dispersal kernel F) and seed losses due to
  predation ( ? ) and other causes ( ? )
• Mass balance equation with one input (the
  dispersal kernel F) and two outputs (seed losses
  ? and ?)

32
7 Model Parameters
a Fecundity, incorporating all pre-dispersal losses
D Mean distance traveled by dispersing seeds
µ Seed mortality not due to predation
ß Total predator number
q Mean distance at which predators are located
Th Handling time
a Searching rate
33
Seed Gains modeled by Dispersal Curve with 2
Parameters

• Seed rain a and mean dispersal distance D
• Effect of increasing dispersal D
• Effect of increasing fecundity a

34
Seed lossespartitioned into two components

• Losses due to Predation depend on number of
  predators, their spatial distribution, searching
  efficiency, and handling times
• Numerical response of predator
• Functional response of predator
• Losses due to all causes other than predation
  (e.g. micro-site limitation) depends on number of
  seeds, spatial distribution, and per capita
  morality rate

35
Full Model of Dynamics of dispersed seeds S at
specific location ? and time t
a Fecundity, incorporating all pre-dispersal losses
D Mean distance traveled by dispersing seeds
µ Seed mortality not due to predation
ß Total predator number
q Mean distance at which predators are located
Th Handling time
a Searching rate
36
Alternative Recruitment Patterns explained by the
model
37
Recruitment patterns obtained by the model

• The plots are based on the following parameter
  setting
• fecundity a 100,
• seed handling time Th 0.1
• mortality not by predation µ 0.1
• searching rate a 5
• predation intensity ß 30
• mean distance of predators q 10
• mean seed dispersal distance
• (a) D 20 (b) D 10 (c) D 3.

38
A Field Guide to Estimating Model Parameters
Parameter Quantity Varies with Empirical Methods
D, a Seed density Distance Field observations (seed traps)
µ Seed mortality not due to predation Distance Field experiments (seed trays protected from predators
q, ß Predator density (N) Distance Field observations (census)
a, Th Seed intake rate Seed density Manipulate seed density in lab and field
P Seed probability to escape predation Distance mortality agents other than seed predators Field observations and experiments
I Density of seeds available for germination Field observations and experiment (seed bank samples)
39
Summary

1. Seeds have distinctive features as a plant
   resource
2. Characteristics of seeds have shaped the life
   styles of consumers as in the fig-bug example
3. Characteristics of seed slayers have shaped seed
   production in plants including seed size and
   number, resistance, timing, and dispersal
4. Unclear to what degree recruitment in plants
   depends on available seeds, microsites for
   establishment, or escape from seed predators