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)

Freshwater Lakes(zooplankton)

Coral Reef(fish)

Kelp Forests(urchins)

Low levels ofgrazing

Naked and/or largephytoplankton

Fast growing, erect, highly palatable algae

Large erect strands of kelp

High levels of grazing

Small phytoplankton or species with reduced vulnerability to

grazing (e.g., gelatinous sheaths)

Slow growing, chemically or morphologically defended algae

(e.g., coralline algae)

Coralline pavements

Herbivore log ratio [ln(NP+/NP-)]

-5 -4 -3 -2 -1 0 1

Pla

nt

log

ra

tio

[ln

(NP

+/N

P-)]

-1

0

1

2

3

marinebenthos

lenticbenthos

lenticplankton

marineplankton

streambenthos

terrestrial

Meta analysis shows big effects of herbivores on plants in marine ecosystemsShurin et al. 2002,Ecology Letters 5:785

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

from Cebrian (1999) Am. Nat. 154: 449-468

Aquatic plants are more nutritious

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

Plants

Predators

Herbivores

Consumers Rule(HSS,1960)

Large consumers are now rare in most coastal ecosystems.

Green turtles

Goliathgroupers

Bluefin tuna

A few examples:

Predators

Herbivores

Plant defenses

Plants

• Morphology (spines or tough tissues)

• Chemicals (secondary compounds)

• Low nutritional (nitrogen content) quality

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

Structural defense = low nutritional value?

High Secondary metabolite content = low N content?

**Multiple defense strategy against generalist herbivore?

Nitrogen content

Structure Chemicals

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 nitrogen-basednitrogen-based toxins.

Secondary metabolites and nitrogen

• Inverse relationship found for some plants (CNBH)

Nutrient limited

High nutrients

High nitrogen

Low secondary metabolites

Low nitrogen

High 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 herbivore-resistant 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) EcologyDuffy 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

Observations

Hypothesis formulation

Experimentation

Interpretation

ConclusionsConclusions

ObservationsObservations

Chthamalus juvenilesChthamalus juveniles

Chthamalus adultsChthamalus adults

BalanusBalanus

ObservationsObservations

Juveniles barnaclesJuveniles barnacles

Adultsbarnacles Adults

barnaclesPredatory WhelksPredatory Whelks

ExampleSpecific 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

LOW Nitrogen0

5

10

15

20

25

30

35

40

80100

No-choice trials

HIGH Nitrogen

Perc

ent T.

testu

din

um

consum

ed /

2 h

0

5

10

15

20

25

30

80

100

LOW Nitrogen

HIGH Nitrogen

Choice trials

p < 0.001

p < 0.01

Madam Margene results!

• Offered bucktooth parrotfishes paired choices between nitrogen-rich and unenriched turtlegrass leaves– 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

Secondary metabolites and nitrogen

• Inverse relationship found for some plants (CNBH)

Nutrient limited

High nutrients

High nitrogen

Low secondary metabolites

Low nitrogen

High secondary metabolites

Seagrass Herbivory: direct evidence of consumption

Urchin Bites

Par

rotf

ish

Bit

es

Response Variables:Grazing Intensity

Area Before Deployment31.90 cm2

Area After Deployment29.05 cm2

Leaf loss = 2.85 cm2

Leaf Loss/Leaf Offered =Grazing Intensity

May 1996

% d

ail

y N

AP

P lo

st/

sh

oo

t

0

100

200

300

400

500

6001200

1400

% b

iom

ass o

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red

re

mo

ved

/sh

oo

t/d

ay

0

5

10

30A

B B

July 1996

0

50

100

150

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350

400

0

2

4

6

8

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14

A

AB

B

November 1996

0

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0.0

0.1

0.2

0.3

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0.5

0.6

Direct estimates find seagrass grazing to be intense

Source: Kirsch et al. 2002. Marine Ecology Progress Series

• On average, some 80% of net aboveground primary production is consumed by small parrotfishes

• In some months grazing exceeded seagrass production

• Grazing varied greatly with season and location

• Herbivores do not graze uniformly across any marine landscape and seagrass are no different!

Hawk Channel

Pickles SmallPatch Reefs

Methodological Issues

• Reliance on static measures as indicators of grazing can grossly underestimate grazing pressure

• Grazing can stimulate Primary Production!

sequential leaf production

increased shootrecruitment &

belowground branching

inaccessible apical& basal meristems

physiological integration high carbohydratereserves

clonal growth

Seagrass Herbivory: seagrass structure and growth may mask grazer impacts

The seagrass grazing paradigm

““In both the saltmarsh and seagrass In both the saltmarsh and seagrass communities, communities, little of the primary little of the primary

production is consumed by herbivoresproduction is consumed by herbivores” ”

C. M. Lalli and T. C. Parsons. 1993. Biological C. M. Lalli and T. C. Parsons. 1993. Biological Oceanography, An Introduction, Pergamon PressOceanography, 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 herbivoreshas led to reducedlevels of seagrass grazing

1. green turtles2. manatees & dugongs3. waterfowl (ducks & geese)

Marine food webs are resilient with high levels of functional redundancy.

Redhead Ducks

Brent Geese Nereid Polychaetes

Sea UrchinsParrotfishes

Various Crustaceans