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Definitions: Herbivory
• Herbivory is a special case of predation
referring solely to the consumption of plants
– herbivory differs from predation in that the
prey are most often only partially consumed,
which is termed grazing (feeding on grasses) or
browsing (feeding on shrubs)
– when seeds are eaten or the entire plant (e.g., a
phytoplankon cell) is consumed, this is
predation
The importance of herbivory to
marine ecosystems
• It is the first step in the transfer of energy in
nearshore food webs
• It provides a major trophic link for the
cycling of nutrients within these food webs
• It often affects the productivity and
structure of plant communities
Anecdotal evidence for the importance
of grazing in marine ecosystems
• Densities of herbivorous fishes can average well
over 10,000 individuals/hectare (Horn, 1989)
• Standing stocks on unfished reefs in the Great
Barrier Reef can reach 45 metric tons/km2
(Williams and Hatcher, 1983)
• In the Caribbean, parrotfishes can graze at rates of
over 150,000 bites per m2/day (Carpenter, 1986).
Community level impacts of herbivores:
what should the evidence look like?
Community Domination
Habitat
(grazer)
Low levels of
grazing
Freshwater Lakes
(zooplankton)
Naked and/or large
phytoplankton
Small phytoplankton or species
with reduced vulnerability to
grazing (e.g., gelatinous sheaths)
Coral Reef
(fish)
Fast growing, erect,
highly palatable algae
Slow growing, chemically or
morphologically defended algae
(e.g., coralline algae)
Kelp Forests
(urchins)
Large erect
strands of kelp
Coralline pavements
High levels of
grazing
Meta analysis shows big effects of herbivores
on plants in marine ecosystems
Plant log ratio [ln(NP+/NP-)]
Shurin et al. 2002,Ecology Letters 5:785
3
2
marine
benthos
lentic
plankton
1
lentic
benthos
0
stream
benthos
marine
plankton
terrestrial
-1
-5
-4
-3
-2
-1
0
Herbivore log ratio [ln(NP+/NP-)]
1
Marine theory is drawn from
terrestrial ecosystems
Important differences between
marine and terrestrial plants
•
•
•
•
Land forms
long lived
slow growing
rich in stored energy
•
•
•
•
Sea forms
short lived
rapid growth
do not store energy
Differences between Primary
Producers
Differences in herbivore size
Aquatic plants are more nutritious
from Cebrian (1999) Am. Nat. 154: 449-468
Herbivory: Why is the world
green?
• Why don’t herbivores consume more of the
plants that are available to them?
– Maybe herbivores aren’t food limited
(predators control herbivore density)
– alternatively the plants are not as available
(palatable) as they appear to us
Hypothesized top-down control
of communities
Consumers Rule
(HSS,1960)
Predators
Herbivores
Plants
Large consumers are now rare
in most coastal ecosystems.
A few examples:
Bluefin tuna
Green turtles
Goliath
groupers
Plant defenses
• Low nutritional (nitrogen content) quality
• Morphology (spines or tough tissues)
• Chemicals (secondary compounds)
Predators
Herbivores
Plants
Plant defense strategies: low
nutritional value hypothesis
• Variance in N content, as expressed by the C/N ratios of
plants, could determine herbivore foraging selectivity
– Simple comparisons of benthic algae and rooted macrophytes
do not support this conclusion
• Moreover the utility of C/N ratios as a predictive tool has never been
verified for marine organisms
• Many marine vascular plants are rich in cellulose and
therefore indigestible
– Differences in gut pH, microbial symbionts and presence of
cellulase in some marine may aid in digestion of otherwise
undefended plants
Herbivores can compensate for
sub-optimal diets
• Physiological mechanisms
– Compensatory feeding: adjustments in feeding rates
and efficiency
– Gut retention time is low
– Metabolic transformations
Linkages between plant
defenses
Nitrogen
content
Structure
Chemicals
Structural defense = low nutritional value?
High Secondary metabolite content = low N
content?
**Multiple defense strategy against generalist herbivore?
Carbon nutrient balance hypothesis
(Bryant 1983)
• The Carbon : Nutrient Balance (CNB) Hypothesis, also known as
the Environmental Constraint Hypothesis, suggests that variation
in plant defense is based on the availability of nutrients in the
environment
– Plants growing in nitrogen-poor soils will use carbon-based
defenses (mostly digestibility reducers), while those growing in
low carbon environments are more likely to produce nitrogenbased toxins.
Secondary metabolites and
nitrogen
• Inverse relationship found for some plants (CNBH)
Nutrient limited
Low nitrogen
High secondary
metabolites
High nitrogen
High nutrients
Low secondary
metabolites
Plant apparency model
• The Plant Apparency Model (Feeny,1976)
has been one of the most influential models
of plant-herbivore interactions.
– This model contrasts two very different types of
plants and seeks to explain apparent differences
in their defense strategies
Plant Apparency Theory
• Plants dominating a community are ‘bound to be found’ by
herbivores (i.e., they are apparent)
• Such plants should invest heavily in generalized defenses that are
effective against a broad range of herbivores
– Polyphenolics (tannins) might fill this role by acting as
digestibility reducers that allowed little counteradaptation by
herbivores. Tannins were termed quantitative defenses because
they were thought to function in a dose dependent manner
• In contrast, fast-growing plants with unpredictable distributions are
unapparent because they are more likely to escape many herbivores
– Because they allocate more resources to rapid growth,
reproduction, and dispersal, unapparent plants should produce
inexpensive toxins (qualitative defenses) that are effective in low
doses against generalist herbivores
Defense Strategies: Secondary Compounds
• Types of chemical defenses:
– quantitative
• examples include tannins and resins which occupy as much
as 60% of a plant’s leaf dry mass
• these compounds were thought to deter specialized
herbivores via reduction of cell wall digestibility. This is
true for vertebrates but not for insects
– qualitative
• comprise < 2% of a plants leaf dry mass
• examples include alkaloids and phenols
• deter generalist herbivores
• are toxins that alter an herbivore’s metabolism, by blocking
specific biochemical reactions.
Plant apparency theory: some
predictions
Marine Plant Apparency
• Predicts that apparent seaweeds such as kelps should have high
levels of phlorotannins relative to less apparent fucales
– Available data show the opposite pattern
• Both within and among genera, phlorotannins are common and
in relatively high abundance in temperate brown algae but almost
completely absent from similar tropical species
– This is opposite of what would be predicted as herbivory is
extreme on tropical coral reefs, and pholorotannins appear to
be effective defenses against tropical herbivores
Examples
Apparent
Less Apparent
Defense Strategies: Morphology
• Types of morphological defenses:
– Tough tissues
• examples include leathery macrophytes such as kelps or
rockweeds
Defense Strategies: Morphology
• Types of morphological defenses:
– Calcified tissues
• Examples include red calcareous algae (L) and tropical algae
such as Halimeda and Penicillus (R)
Associational Defenses
An associational defense is protection
gained by an organism from living in
association with another species.
Associational Refuges
• Palatable seaweeds can persist in
herbivore-rich communities if they
grow on or beneath herbivoreresistant competitors
– A number of palatable
seaweeds can be found under
the canopy of Stypopodium
zonale (see picture)
– Palatable algae can be found
under unpalatable seaweeds like
Sargassum filipendula
Strong Dictyota preference by
amphipods reduces predation risk
from pinfish
Duffy and Hay (1991) Ecology
Duffy and Hay (1994) Ecology
Herbivores such as ascoglossan gastropods
sequester algal toxins and use them as
defenses from predators
Moon Snail
Blue Sea Slug
Sea Hare
Additional evidence from the
Study of Marine Communities
• Investigation and description of community
pattern
• Any study of interacting species is a community
level study
• Investigations of the processes that determine
community properties
The Scientific Method
Conclusions
Interpretation
Experimentation
Hypothesis formulation
Observations
Observations
Chthamalus juveniles
Chthamalus adults
Balanus
Observations
Juveniles barnacles
Adults
barnacles
Predatory Whelks
Example
Specific plant and animal (invertebrate)
McGlathery 1995—No
relationship; ate similar amounts
in eutrophied vs. uneutrophied
sites
Valentine and Heck 2001—
negative relationship; ate more of
low nitrogen than high nitrogen
Alternative examples
Bjorndal 1985—Positive
relationship; feeding plots
revisited
Madam Margene’s thesis work: Sparisoma
radians -bucktooth parrotfish
• Model herbivore
• Resident of Caribbean
grass beds
• Feeds at nearly
constant intensity
throughout the day
• Prefers T. testudinum
Madam Margene results!
– Results of these lab
experiments and field
experiments showed that
when given a choice, these
herbivores consistently
choose high nitrogen plants
• Perhaps herbivores are not
as dumb as they look
100
80
40
Choice trials
35
p < 0.001
30
25
20
15
Percent T. testudinum consumed / 2 h
• Offered bucktooth
parrotfishes paired choices
between nitrogen-rich and
unenriched turtlegrass
leaves
10
5
0
HIGH Nitrogen
LOW Nitrogen
100
80
30
No-choice trials
p < 0.01
25
20
15
10
5
0
HIGH Nitrogen
LOW Nitrogen
Secondary metabolites and
nitrogen
• Inverse relationship found for some plants (CNBH)
Nutrient limited
Low nitrogen
High secondary
metabolites
High nitrogen
High nutrients
Low secondary
metabolites
Parrotfish Bites
Seagrass Herbivory:
direct evidence of consumption
Urchin Bites
Response Variables:
Grazing Intensity
Area Before Deployment
31.90 cm2
Area After Deployment
29.05 cm2
Leaf loss = 2.85 cm2
Leaf Loss/Leaf Offered =
Grazing Intensity
Direct estimates find seagrass
grazing to be intense
A
30
May 1996
500
10
400
300
5
200
% daily NAPP lost/shoot
100
B
B
0
400
350
300
250
200
150
100
50
0
30
• Grazing varied greatly with
season and location
July 1996
B
0
14
12
10
8
6
AB
4
A
2
0
0.6
November 1996
25
0.5
20
0.4
15
0.3
10
0.2
5
0.1
0
0.0
Hawk Pickles Small
Channel
Patch Reefs
% biomass offered removed/shoot/day
1400
1200
600
• In some months grazing
exceeded seagrass production
• On average, some 80% of net
aboveground primary
production is consumed by
small parrotfishes
• Herbivores do not graze
uniformly across any marine
landscape and seagrass are no
different!
Source: Kirsch et al. 2002.
Marine Ecology Progress Series
Methodological Issues
• Reliance on static
measures as indicators
of grazing can grossly
underestimate grazing
pressure
• Grazing can stimulate
Primary Production!
Seagrass Herbivory: seagrass structure and
growth may mask grazer impacts
sequential leaf
production
increased shoot
recruitment &
belowground branching
inaccessible apical
& basal meristems
physiological integration
clonal growth
high carbohydrate
reserves
The seagrass grazing paradigm
“In both the saltmarsh and seagrass
communities, little of the primary
production is consumed by herbivores”
C. M. Lalli and T. C. Parsons. 1993. Biological
Oceanography, An Introduction, Pergamon Press
Plankton- Zooplankton
• Copepods, tiny crustaceans
about the size of a grain of rice,
• Copepods are the primary
herbivores in the water column
making up some 70-90% of
herbivore biomass
• Copepods are a primary food
source for the larval fish.
Food Web Alteration Hypothesis
Historical overharvesting of large vertebrate
herbivores
has led to reduced
levels of seagrass grazing
1. green turtles
2. manatees & dugongs
3. waterfowl (ducks & geese)
Marine food webs are resilient with
high levels of functional redundancy.
Parrotfishes
Redhead Ducks
Brent Geese
Various
Crustaceans
Sea Urchins
Nereid Polychaetes