OIKOS 86: 3-15.

Copenhagen 1999

Why are parts of the world green? Multiple factors control

productivity and the distribution of biomass

Gary A. Polis

Polis. G. A. 1999. Why are parts of the world green? Multiple factors control
productivity and the distribution of biomass. Oikos 86: 3-15.
-

This paper evaluates the multiple factors that determine the production of plant
biomass and its distribution among producers and various trophic groups of con-
sumers. In rough order of their importance, water and nutrient availability, factors
that deter herbivores (plant defenses, environmental heterogeneity and disturbance,
nutrient stoichiometry), and consumption by herbivores appear to be the most
universal determmants of the production and distribution of plant biomass. In some
times and places, indirect effects from enemies of herbivores (predators, parasites,
parasitoids and pathogens) propagate through the food web to influence plant
biomass, in a manner somewhat consistent with green world and exploitation
ecosystem mechanisms. I discuss why such food web dynamics appear to be much
more important in water than on land. The only demonstrated cases of community-
level trophic cascades occur in water. Although species-level cascades are moderately
frequent on land, community-level cascades rarely or never occur.

G. A. Polis, Dept of Encironrnental Sciences and Policy, Unic. o f Califbrnia, Dii~.is,CA

95616, U S A (gapolis@ucda~~is.e~~u).
Primary productivity is among the most fundamental
biological processes on the planet, transferring the en-
ergy locked in light and various inorganic molecules
into forms useful to sustain producers and the diversity
of consumers. What factors control primary productiv-
ity and regulate its distribution among plants, animals,
and microbes? How do changes in primary productivity
work their way through a food web to alter the abun-
dance and biomass of herbivores to predators and
detritivores? Answers to these questions carry great
importance, not only to the structure of communities
and the dynamics of ecosystems but to such practical
considerations as the success and conservation of key
and endangered species and yields of world fisheries
and agriculture.
Colors of the world
As a didactic exercise, I take the reader on a chromatic
tour of our world to examine, from several perspectives,
This is an invited Minireview on the occasion of the 50th
anniversary of the Nordic Ecological Society Oikos.
Copyright O OIKOS 1999
ISSN 0030-1299
Printed in Ireland - all rights reserved
its colors. I do this for two reasons. First, this approach
offers insight into the multiple abiotic and biotic factors
that control the most basic elements of communities
and ecosystems: the regulation of primary productivity
and the distribution of biomass among plants and
animals. Second, two enduring hypotheses highlight
color in their explanation of biomass distribution. The
"green world" hypothesis (GWH), in its most basic
form, proposed that the world is green, primarily be-
cause herbivores, held in check by their enemies, do not
consume a large fraction of plant biomass. The ex-
ploitation ecosystem hypothesis (EEH) stressed that
varying productivity, herbivory, and predation make
habitats green in systems with one or three trophic
levels but "barren" in systems with two or four levels.
The editors of Oikos asked me to assess these hypothe-
ses and I do so towards the end of this paper. I first
place these hypotheses in a larger context by suggesting
that GWH and EEH processes are one of many factors
that explain the distribution of biomass within
con~munities.
Colors from space: the global influence of abiotic
factors
If one views the world from space, it is multi-colored.
The land, white at the poles, becomes green in boreal
latitudes and through parts of the tropics, and grades
red to brown in the deserts and savannas; all is
framed by great expanses of blue water. The distribu-
tion of these habitats reflects the broad and over-
powering influence of climate and incident solar
radiation on patterns of annual net primary produc-
tivity (ANPP) and plant biomass. These factors
largely determine the general latitudinal distribution
of deserts, tropical forests, taiga. tundra. and ice
fields; within a latitudinal zone, these factors are ma-
jor determinants of the transition of vegetation types
(e.g., forest +tall grass prairie + short grass prairie +
desert).
Primary productivity on land is a function of temper-
ature and tightly correlated with precipitation (Jenny
1941, Polis 1991b, Bradley and Weil 1996, Polis et al.
1997a. b). Temperature, water, and potential evapo-
transpiration constrain ANPP from 3 to < 100 g C
m -'yr - and minimize the accumulation of soil or-
ganics and nutrients in "barren" deserts, be they polar
or semi-tropical. We see much "green" only when
climatic and light factors are appropriately benign:
grasslands and forests, from boreal to tropical, receive
sufficient water and light to facilitate relatively high
ANPP (600- > 3000 g C m 2 y r ' ) (Whittaker 1975).
Iwzplication: The most parsimonious explanation is
that sunlight and climate largely determine the
"greenness" of the world.
Catastrophes and El Niiios: abiotic disturbances
powerfully determine greenness
The earth's history is punctuated by events of such
magnitude that the fundamental nature of biological
communities and ecosystems are radically and irre-
versibly changed worldwide. At least 10 mass extinc-
tions are recognized during the last 250 MYr. Two
such catastrophes were so profound they mark the
transition among the three major periods of life. The
Yucatan asteroid 65 MYrBP wiped out about 75% of
all species and marked the end of the Mesozoic. Al-
though the direct effects (explosion, vaporization and
burning of forests, tsunamis) immediately eliminated
many species, a great cloud of dust injected into the
atmosphere initiated a prolonged global winter that
reduced light, lowered temperatures, and likely halted
most photosynthesis worldwide. This drastic drop in
ANPP worked up the food web to eliminate most
consumer species. Massive extinctions (70% and 90%
of land and marine species) also marked the end of
the Paleozoic 250 MYrBP. Evidence (Renne et al.
1995) suggests that a millennium of volcanic eruption
at the Siberian shield darkened the atmosphere and
cooled the earth sufficiently to reduce ANPP to such
low levels that most life perished. Lesser events (e.g..
global cooling and darkening from the 1887 Krakatoa
explosion) also can reduce ANPP. both locally and
globally.
Other physical events that alter climate. control
ANPP, and determine greenness occur more regularly,
but at shorter time scales. Ice ages and the accoinpa-
nying global aridity are obvious examples that de-
crease productivity and green biomass worldwide. At
an even shorter scale, cyclical El Niiio events change
community structure and productivity over a large
part of the globe. Through its effects on upwelling
and consequent nutrient availability, El Niiio strongly
affects marine ANPP throughout the Pacific (Glynn
1988). Through its effects on precipitation, El Niiio
strongly affects productivity and community dynamics
in many terrestrial systems - it can bring drought
and crop failure to Australia and Indonesia while,
concurrently, increasing ANPP along the west coast
of the Americas (Polis et al. 1997a, b).
Itnplicatiorz: Large-scale disturbances at various tem-
poral scales further demonstrate that light and cli-
mate are among the most powerful forces controlling
ANPP, plant biomass, and resultant community struc-
ture.
Blue oceans and colored soils: the influence of
nutrients
Our oceans and most great lakes appear blue, a
reflection that the world's waterways are generally not
very productive and contain little standing biomass.
The color of the water depends on the concentration
of algae, and which species are present. Clear and
unproductive water reflects ultraviolet and blue light;
algal photosynthetic pigments absorb these colors. Al-
though several factors contribute to low productivity
in great bodies of water, two stand out: severe light
and nutrient limitation. There is insufficient light for
photosynthesis resulting in near zero ANPP for the
> 97.5% of the ocean below the compensation depth
of plants.
Nutrient limitation is generally much more severe in
water compared to land; nutrients are not readily avail-
able in "top soil" as they are for land plants (Valiela
1984. Barnes and Hughes 1988). The richest ocean
water has 0.00005% N ( = 1 10000 of N in top soil).
Thus, mean ocean productivity (69 g C m - ' y r ') is
about 20%)of mean ANPP on land (324 g C) (Lieth and
Whittaker 1975, Whittaker 1975. Lieth 1978, Valiela
1984). Such low nutrient levels cause a large part of the
world's open oceans to be "blue deserts" with extremely
low ANPP (10-50 g C m - 2 y r ' ; e.g., most tropical
waters, central gyres). In fact. total ANPP for oceans is
only 25-30% of theoretical maximum based on light
availability. Only where nutrients are available (up-
welling areas and those with terregenous input) does
ANPP approach or exceed terrestrial systems (e.g.,
500- > 3500 g C m - 2 yr- ') and plankton filled waters
become less transparent and less blue. When nutrients
are "over-available", water bodies become eutrophied
and change colors, e.g., "red tides" (dinoflagellate
blooms that also are yellow and brown) or "pea-soup"
green eutrophied lakes. Overall, nutrients affect "green-
ness". or lack thereof, in open oceans, bays, coral reefs,
kelp forests, the rocky intertidal, and salt marshes, as
well as lakes, streams, and temperate and tropical
("whitewater" vs "blackwater") rivers (references in
Polis and Strong 1996).
Nutrients also affect ANPP and the color of terres-
trial habitats from forests to deserts and grasslands
(Tate 1987, Running and Hunt 1993, Polis and Strong
1996). Areas with high ANPP are characterized by dark
soils, rich in organic matter and associated nutrients,
particularly nitrogen (Tate 1987. Bradley and Weil
1996). Many parts in the world with low ANPP and
crop yields are nutrient limited (Huston 1993). These
areas produce and retain little organic carbon and
inorganic minerals dominated soils (Tate 1987, Bradley
and Weil 1996). Such edaphic conditions provide won-
derful displays in hot deserts: red rocks and pink soils
from iron oxide, and white carbonate sands. The red
oxisol soils exposed when many tropical forests are
destroyed reflect the great nutrient limitation in these
systems (Vitousek and Sanford 1986), especially after
the system's nutrients are burned or hauled away as
crops, lumber and livestock (Bradley and Weil 1996). It
is now clear that our verdant tropical forests are cru-
cially dependent on allochthonous nutrients: e.g., the
Amazon forest remains productive and green only be-
cause it receives most of its phosphorus from dust
originating in Africa (Swap et al. 1992). Likewise. al-
lochthonous nutrients deposited by water through time
promote the rich, dark to black humus soils and high
ANPP that characterize floodplains. "bottom lands",
fertile deltas, and other high yield agricultural areas.
Nutrient limitation in water may also affect patterns
of biomass production on land. Nutrient limitation is
now implicated in cycles of global warming and cooling
(Behrenfield and Kolber 1999). When iron and possibly
other nutrients are supplied by windblown input from
arid lands during cool periods, oceanic productivity
increases and more CO, is removed from the atmo-
sphere, thus exacerbating the cooling trend, increasing
aridity, and decreasing productivity.
Implication: Within the abiotic constraints of water,
temperature, and light, nutrients limit productivity
across most habitats and are a very large part why the
world is a productive green, or a barren blue or red.
Humans demonstrate how planetary color is
influenced by nutrients and water
It would be delinquent to omit the power of humans to
alter ANPP and biomass distribution worldwide (Vi-
tousek 1994, Vitousek et al. 1997). Humans shift colors
in both directions: green tolfrom blue;brown,red. Irri-
gation and,'or nutrient fertilizer subsidies have made
many "marginal" areas into productive agrosystems,
bursting with greenness (e.g., California and Israeli
deserts). Projections of global warming and increases of
biologically useful atmospheric N predict that human
activities will greatly increase the ANPP and greenness
of many communities worldwide (Vitousek 1994, Vi-
tousek et al. 1997). Runoffs of N and P change the
colors of many waterways as ANPP increases and a
variety of benign to noxious algae dominate these
systems.
Humans reduce greenness in many places. As an
extreme, too much ANPP from anthropogenic N and
P have severely degraded many aquatic systems, pro-
ducing > 50 "deadzones" worldwide that sustain only
anerobic microbes. On land, poor farming practices.
cropping, overgrazing, logging, fires, and consequent
erosion of top soils repeatedly have reduced available
nutrients and organics and depressed sustainable
ANPP (Bradley and Weil 1996). Degradation range
from desertification of large areas (e.g., Iraq's fertile
crescent - from the cradle of civilization to site of
desert wars), to conversion of our great forests and
grasslands to rangeland, fertilizer-subsidized farmland,
or unproductive habitats (as seen in Europe, Africa,
India, Asia, and the pantropics). These changes, which
greatly reduced soil organics and nutrients from their
pristine state (Tate 1987). have converted much of our
green habitats and dark soils to other colors (e.g., to
pale yellow green of nutrient-stressed vegetation and
the reds and whites of desert aridsols) (Bradley and
Weil 1996).
Changes can even be seen from space. About 10000
YrBP, forests occupied an estimated 70-80% of the
-
ice-free land surface; in 1500 BP, forests occupied
33%. Via human activities and climate change (global
warming), forests have been gradually reduced to 17-
20% (at the current rate of destruction [estimated at ca
75000 acres'day], < 15% is projected to remain by
2020). At the same time, deserts are growing and now
occupy 25-30% of the land's surface. These changes
suggest a truly amazing observation: during the expo-
to a current -
nential increase in humans (from 5 million 10000 YrBP
6 billion), earth's macro-description has
degraded from a green "Forest planet" to a red-brown
"Desert planet".
Implication: Human activities, causing loss or gain of
organics and nutrients, are major reasons why parts of
the world are green, whereas other parts are barren.
Geology in black and white: herbivores eat a
small fraction of ANPP
Earth scientists emphasize that the history of life is
revealed in rocks and soils. Indeed, a primary goal of
paleoecology is to discern the structure, processes and
function of ancient communities and ecosystems.
Worldwide, in strata from many ages, huge deposits of
fossil plants suggest that herbivores have not kept pace
with plant production for a long time. It now appears
that "macro-herbivores" were a negligible player in
terrestrial systems until at least the Upper Carbonifer-
ous; most plant productivity went directly to detriti-
vores (P. Seldan pers. comm.). Indeed, the great loss of
habitat and biodiversity over the last century has been
temporally subsidized by fossil fuels - (black) coal and
oil are the legacy of plant C-C bonds unbroken by past
herbivores (or detritivores).
More recent failures of consumers to deplete past
productivity are illustrated by widespread peat bogs,
the extensive and deep deposits of rich organic top soil,
and the organic ooze that covers much of the ocean
floor. More organic carbon is stored in the soil than
in the world's vegetation and atmosphere combined
(Bradley and Weil 1996). Corals, another set of uneaten
fossil primary producers (about half photosynthetic
dinoflagellates by mass), form massive (white) deposits
in tropical seas. Foraminifera, another symbiotic au-
totroph, also form great deposits (e.g., the white cliffs
of Dover). Large areas of the sea floor are covered with
deep deposits of uneaten marine autotrophs (diatoms,
dinoflagellates, radiolariaus, foraminifers).
Implication: Past herbivores and detritivores did not
consume a large quantity of ANPP.
Table 1. Estimates of annual net primary productivity (ANPP), standing plant biomass, and consumption by herbivorous
animals in terrestrial, marine, freshwater systems and the entire 510 x lo6 km2 planet Earth. These data are from Whittaker
(1975) and Lieth and Whittaker (1975). YoANPP consumed (*) is from Cyr and Pace 1993.
Area (%) Plant biomass
(10" metric tons C)
Land 29 82.7
Ocean 70.8 0.176
Lakes and streams 0.1 0.002
Total planet 82.9
6 OIKOS 86 1 (1999)
Modern terrestrial herbivores likewise usually
consume little ANPP
On average, less than a fifth of ANPP on land is eaten
each year (Cyr and Pace 1993, Polis and Strong 1996,
Crawley 1997; Table l), with the rest remaining as
standing plant biomass or becoming detritus. Indeed,
the 17 x ratio of standing biomass (SB) of plants com-
pared to their ANPP clearly shows that terrestrial
herbivores leave a great amount of tissue uneaten
(Table 1). Moreover, land ANPP and standing biomass
generally follow predictions of models based purely on
abiotic factors (light, temperature, precipitation, poten-
tial evapotranspiration; Lieth 1978, Running and Hunt
1993). This strongly suggests that grazing plays a com-
paratively minor role for land plants on a global scale,
although herbivory may be quite important at finer
scales (McNaughton 1998, see next section).
Implication: Extant terrestrial herbivores normally take
a small fraction of ANPP.
Insects and ungulates: the great potential
influence of herbivores on land
It is clear that herbivores can often control land plant
community composition (Crawley 1989, McNaughton
1998). Moreover, herbivores sometimes consume a
large portion of ANPP (range: < 1% to > 90%, mean:
18%; Cyr and Pace 1993, McNaughton 1998; also see
Table 1). transferring plant biomass into a large stand-
ing biomass of animals, e.g., in the Serengeti (Mc-
Naughton 1998). Nevertheless, even such heavily
grazed systems with high secondary productivity main-
tain substantial standing plant biomass (Whittaker
1975).
Dramatic examples of "runaway consumption" (i.e.,
herbivores leave little standing plant biomass, Strong
1992) exist. These include the periodic outbreak of
defoliators (e.g., gypsy moths or migratory locusts) and
overgrazing by introduced animals (sheep on islands or
rabbits in Australia). Introduced grazers can change the
structure of plant communities, selectively removing
many species, including most saplings), thus converting
ANPP Ratio U/;, ANPP consumed
Biomass!ANPP
4.83 17.1 7 (18*)
2.49 0.071 37
0.06 0.033 20 (51*)
7.32 11.3 17
a forested area into a savanna, grassland, or even desert
(Crawley 1989, 1997). The money and effort devoted to
control pests is strong testament that herbivores can, on
occasion, decimate crop ANPP. Worldwide, it is esti-
mated that insects take about as much crop production
as is used by humans.
Iinplication: Terrestrial herbivores have the ability to
reduce standing plant biomass and thus "greenness", at
least in some times and places.
Inverted pyramids: the great influence of
herbivores in aquatic systems
In contrast to land, herbivores are a more important
determinant of plant standing biomass (SB) in aquatic
systems. On average, they take 51% of ANPP (Cyr and
Pace 1993). The frequent existence of "inverted biomass
pyramids" in freshwater systems (Wetzel 1975) reflects
that herbivores often monopolize more SB than produc-
ers. The same inverted SB distribution characterizes the
ocean in many times and places, e.g., temperate copepods
(Parsons and Lalli 1988), intertidal (Bustamante et al.
1995) or subtidal (urchin barrens) grazers. In marine and
freshwater systems as a whole, plant SB only represents
an estimated 3-7% of ANPP (Table I).
Implication: Herbivores often influence patterns of
biomass, and reduce "greenness" in many aquatic sys-
tems, especially as compared to their terrestrial
counterparts.
What limits the capacity of herbivores to
regulate plant biomass?
These general observations suggest several questions.
Why don't herbivores eat more ANPP? Why do herbi-
vores have such variable effects on plant biomass among
habitats and between water and land? Here, I explore six
hypotheses to assess the variable factors that affect the
capacity of herbivores to regulate plant biomass, the sixth
being the Green World and Exploitation Ecosystem
Hypotheses. Undoubtedly and most realistically, each of
these six contributes, alone and in combination to
constrain herbivores; all are important in different times
and places.
1. Plants are not passive agents, waiting to be
decimated by herbivores
The apparently verdant forests of the tropics and temper-
ate zones are actually primarily brown by weight, reflect-
ing that most biomass is woody lignin, rather than green
OIKOS 86.1 (1999)
chlorophyll. The indigestibility of lignin and cellulose to
higher animals and the effectiveness of the myriad
(structural, chemical, phenological) ways in which plants
reduce herbivory are well known (Coley et al. 1985).
Likewise are the well-known arguments that plant de-
fenses limit herbivory, thus allowing a green world
(Ehrlich and Birch 1967, Strong 1992, Polis and Strong
1996).
However, defenses are not universal; all plant species
are still vulnerable, at least to specialists. Thus, defenses
only restrict herbivore effectiveness by decreasing rates
of discovery, consumption, or digestion. The question
remains, why does not some subset of herbivores deci-
mate plant biomass everywhere and always? I suggest
below that plant defenses act in concert with other factors
to decrease herbivore consumption.
In aquatic systems, many plants are likewise well
defended (e.g., coralline algae, armored and toxic phyto-
plankton, chemicals in macroalgae; e.g., Liebold 1989);
such defenses often limit herbivores from depressing
plant biomass (e.g., symbiotic zooxanthellae in corals;
noxious freshwater blue-green algae). Liebold et al.
(1997) suggest the generality that more defended plant
species increase with increasing productivity so that most
plant biomass is well defended in productive systems.
Nevertheless, in most systems, a subset of herbivores
likely has the ability to bypass these defenses. Herbivores
are sometimes so effective that plant biomass can be
driven to low levels (e.g., urchins on kelp, copepods on
temperate phytoplankton, Daphnia on lake phytoplank-
ton, midge larvae on stream algae).
2. Nutrients, not carbohydrates, limit herbivore
numbers, and thus their effects
Animals require both energy and a variety of "nutritional
requisites" to grow, complete their life cycle, and repro-
duce. Important nutrients include nitrogen, phosphorus,
some trace elements, fatty acids, and vitamins. N is an
integral component of many essential compounds - it is
a major part of amino acids, the building blocks of
protein, including the enzymes that control virtually all
cellular processes. Other N compounds include nucleic
acids and chlorophyll. P is used for adenosine triphos-
phate (ATP - the energy currency of all cells), nucleic
acids (DNA, RNA), and phospholipids, particularly in
cell membranes.
The availability of nutritional requisites constrains
growth and reproduction in virtually every species
(White 1993, Sterner and Hessen 1994, Elser et al. 1996,
Brett and Muller-Navara 1997). N and P are particu-
larly important. The ratio of C/N in plants range from
10,l to 3011 in legumes and young green leaves to as
high as 600! 1 in some wood (Bradley and Weil 1996).
The C;N ratios in animals and microbes are much
lower, ordinarily falling between 5/1 and 1011. Such
differences in C'N ratios between plants and their
consumers lower the rate of decomposition by microbes
(Bradley and Weil 1996) and herbivory by Metazoa. In
Tlze Inadequate Environment, White (1993) provides
ample evidence that heterotrophs chronically lack ade-
quate N to grow or reproduce optimally (also see
Sterner and Hessen 1994, Elser et al. 1996, Polis and
Strong 1996). The importance of nutritional restriction
is reinforced by the foraging literature that clearly
shows that herbivores choose their foods based on
nutrient as well as energy content.
In many cases, P availability constrains herbivore
success. The Redfield Ratio describes the approximate
stoichiometric mix (1 10 C : 250 H : 75 0 : 16 N : 1 P) of
elements essential to organisms. In particular, the N,'P
ratio crucially determines productivity and species com-
position (Elser et al. 1996). Thus, energy (C-C bonds)
and N could be abundant, but neither individuals nor
populations grow maximally because P is insufficient.
As P is essential to cell division (and thus reproduc-
tion), a high N,IP ratio especially limits the growth of
organisms that have high potential r,,,, such as most
herbivores and detritivores. These organisms are key to
the potential regulation of plant biomass (and detritus).
Evidence now suggests that high NIP ratios can impede
trophic cascades (Elser et al. 1996). Daphnia, a key to
many lake cascades, respond sufficiently rapidly to
phytoplankton productivity to depress plant biomass.
In lakes with inadequate P, slower growing copepods
replace Daphnia; these copepods do not have the repro-
ductive capacity to depress phytoplankton biomass.
We are beginning to understand how stoichiometry
and nutritional balance affect population and food web
dynamics (Sterner and Hessen 1994, Elser et al. 1996,
Brett and Muller-Navara 1997). Nevertheless it is ex-
tremely likely that herbivore growth is often less than
maximal solely because the environment does not
provide sufficient quantities of all key nutritional requi-
sites. In fact, the greatest disparity in biochemical,
elemental, and stoichiometric composition in the entire
food web occurs at the link where herbivores convert
plant material into animal tissue (Sterner and Hessen
1994, Elser et al. 1996, Brett and Muller-Navara 1997).
The implication is clear: even in a world full of green
energy, manylmost herbivores cannot obtain enough
requisite resources to grow, survive, or reproduce at
high rates. Nutritional shortages regulate herbivore
numbers. often limit their effects on plant biomass, and
form one important reason why much of the world is
green.
3. Abiotic factors (climate, disturbance) limit
herbivore numbers to observed levels
In mostlall habitats during most time periods, herbi-
vore populations are depressed to some extent by the
intercession of abiotic factors that stunt growth or
cause substantial mortality. These include extreme tem-
peratures (heat, freezes), water availability (drought.
soil over-saturation), floods (inundation, salinity
changes in coastal waters), fires, scouring (by ice,
floods), transport to unfavorable environments (insects
by wind, zooplankton by moving water), and severe
storms with strong winds and wave action. Each factor
can disturb otherwise deterministic consumer-resource
interactions and depress herbivore numbers below lev-
els that decimate plant biomass. The central role of
climate and disturbance as key determinants of con-
sumer number and success is an old, but nonetheless
quite valid proposition, best advocated by Andrewartha
and Birch (1954, 1984) and articulated by many others
(e.g., Ehrlich and Birch 1967, Dunson and Travis 1991,
Polis 1991b, 1994).
4. Spatial and temporal heterogeneity
All communities are markedly heterogeneous through
time and space. Productivity, distribution, abundance,
species composition, and species interactions are vari-
able at scales from centimeters to kilometers and from
days to seasons and years to centuries. Such variation
significantly influences many key processes and is cen-
tral to our understanding of communities (Wiens et al.
1986, Giller and Gee 1987, Polis 1991b, Polis et al.
1996). Thus, neither trophic relationships nor food web
dynamics and structure are constant in space or time
(Polis et al. 1996, 1997a, b). Such variation produces
rather dynamic, non-equilibrium communities (Wiens
1977. Polis 1991b) and allows persistence and coexis-
tence among species that would be excluded by other-
wise deterministic interactions (Caswell 1978, Taylor
1988). It is likely that spatial and temporal heterogene-
ity frequently inhibit a universal or even widespread
outcome of any particular consumer-resource interac-
tion, including the ability of herbivores to depress plant
biomass.
5. Herbivores limit their own numbers
Herbivores engage in many types of negative interac-
tions, both intra- and inter-specific (e.g., cannibalism,
territoriality, fouling, intraguild predation, exploitation
competition: Polis 1981, 1988, Polis et al. 1989, Denno
et al. 1995). Such interference and competition impose
density-dependent limits on consumer abundance (Bed-
dington et al. 1978, Polis 1981, 1988, Arditi and
Ginzburg 1989, Polis et al. 1989, Skogland 1991). It is
clear that such self-regulation constrains the potential
of consumers (e.g., herbivores) to depress their re-
sources (Gatto 1991, Polis and Holt 1992, Polis and
Strong 1996, Holt and Polis 1997).
6. Predators constrain the capacity of herbivores
2 million annu-
to regulate plant biomass
Consumers often depress the abundance or biomass
of their resources, be they herbivores on plants or
predators on herbivores. Such recipient control forms
the root of the Green World (Hairston et al. 1960,
Slobodkin et al. 1967, Hairston and Hairston 1993,
1997) and Exploitative Ecosystem (Oksanen et al.
1981, Fretwell 1987) Hypotheses (GWH, EEH). Here.
consumers form aggregated "trophic levels" that are
posited to regulate the biomass of the trophic level on
which they feed. Thus. the world, for the most part,
is "green" because herbivores. held in check by their
enemies, do not overexploit plant biomass (Hairston
et al. 1960. Slobodkin et al. 1967). This view was
modified by EEH to explain why some habitats sup-
port little plant biomass. EEH herbivores are not al-
ways regulated. If predators do not form an effective
trophic level, herbivores can depress plant biomass.
Predators are not efficient either because productivity
is too low to support a predator trophic level or
sufficiently high to allow predators of predators to
limit them (Oksanen et al. 1981, unpubl., Fretwell
1987). Likewise. Hairston and Hairston (1993) ex-
panded G W H thinking to four trophic level systems.
Note that such consumer control is the most elabo-
rate explanation of patterns of plant biomass. G W H
and EEH require three strong interactions to act in
concert through the food web: herbivores depress
plants; predators depress herbivores; predators thus
indirectly facilitate plants (four levels need five strong
interactions). The other five processes involve only
one direct interaction (i.e., plant defenses) or two
steps (e.g., nutrients or climate limit herbivores di-
rectly. thus facilitating plants). On these grounds
alone. I expect that GWHIEEH control of plant com-
munity biomass is less frequent than control via the
other factors.
Four classes of speciose and abundant consumers
eat herbivores: predators. parasitoids, parasites, and
pathogens (PPPP). Predators are well represented in
most habitats, both in terms of species and abun-
dance. The numbers and diversity of parasitoids are
astounding - parasitoid-host interactions involve an
estimated half of all Metazoan species (Hawkins and
Gross 1992). An average of 10 parasitic worm species
inhabit each vertebrate host population in North
America, with individual hosts averaging > 350 indi-
vidual parasites (Dobson and Hudson 1986, Dobson
et al. 1992). Pathogens - virus, rickettsia, bacteria,
and sporozoans - are likewise speciose and, at least
during outbreaks, astronomically numerous (Anderson
and May 1978, McDonald et al. 1989).
Undoubtedly, consumers decrease the success and
abundance of every multicellular species on the
planet. For example, malaria resides in an estimated
500 million Homo sapiens, killing -
ally. Non-native predators often devastate elements of
the native fauna (e.g., on islands, Towns 1991). Many
studies also show that PPPP often shape the evolution
(e.g., defenses, life history), behavior, species composi-
tion, distribution, and ecology of their resources (An-
derson and May 1978, Dobson and Hudson 1986,
Crawley 1993, Vermeil 1994, Liebold et al. 1997).
Less evidence suggests that predation depresses her-
bivores sufficiently to allow trophic cascades of com-
munity biomass, as proposed by GWH and EEH (see
next section). This statement appears quite robust for
terrestrial systems (Crawley 1989, Hunter and Price
1992, Strong 1992, Polis 1994. Polis and Strong 1996,
Polis et al. 1997a, b), but has many exceptions in
aquatic systems. A prima facie argument is that herbi-
vore fluctuations are often somewhat independent of
PPPP abundance - outbreaks generally do not appear
to be tightly correlated with changes in PPPP num-
bers (NB, consumers sometimes suppress outbreaks).
Moreover. we are in the midst of a terrible experi-
ment that adds little credence to G W H or EEH con-
cepts. The extirpation of top vertebrate predators
worldwide has not caused obvious general effects that
travel to herbivore abundance and lead to changes in
"color" (plant biomass) for most habitats.
Although PPPP are speciose and abundant, they
appear to regulate herbivore biomass only sporadi-
cally. What limits them and blunts their capacity to
control? Logic suggests and data show that these con-
sumers are held in check by the same diverse factors
that limit herbivores: resource defenses, inadequate
nutrients, disturbance, abiotic factors. spatial and
temporal heterogeneity. self-regulation, and their
predators (see Polis et al. 1989, Polis 1991a, Polis and
Holt 1992, Polis and Strong 1996. Polis et al. 1998).
Only when and where these often quite strong con-
straints relax, can PPPP become effective G W H or
EEH agents to alter community-wide patterns of
plant biomass.
Why do trophic cascades occur?
Consumer control of plant biomass does occur on
occasion, as clearly evidenced by the community-level
trophic cascades in water. I suggest that three general
sets of factors enable the intercession of consumer
control and facilitate cascades that affect community
biomass.
1. Appropriate extrinsic environmental conditions
Community-wide effects via consumption by keystone
species are quite context-dependent, occurring only
under very particular conditions (Strong 1992, Menge
et al. 1994, Brett and Goldman 1996, Power et al. 1996,
Liebold et al. 1997). The well known cascades in lakes
(Carpenter and Kitchell 1993, Brett and Goldman 1996,
Elser et al. 1996) and rivers (Power 1990, pers. comm.)
only occur in some times and places. Many factors need
occur to allow lake cascades (Liebold 1989, Carpenter
et al. 1992, Carpenter and Kitchell 1993) (also see
section Differences in consumer control between water
and land). For example, nutrient status appears to be a
key to allow,suppress cascades (Elser and Goldman
1991, Strong 1992, Elser et al. 1996).
The overriding point is that environmental condi-
tions must be "right" for full-blown, community-level
cascades to occur (i.e.. produce dramatic changes in
plant biomass: also see extensive qualifications in
Hairston and Hairston 1993, 1997, Oksanen unpubl.).
Thus, important questions become: What are the ap-
propriate conditions? How frequently do they occur?
Are they general or system-specific? I suspect that the
great spatial heterogeneity and temporal variability that
characterize most systems constrain cascades to a few
places during a few times when the proper conditions
conjunct. Thus, in my view, cascades that change the
community-wide distributions of biomass are an excep-
tional event rather than universal or normal.
2. Intrinsic characteristics of key consumers and
resources
It appears that only some consumers have the innate
capacity to become strong top-down agents in their
communities (see section Differences in consumer con-
trol between water and land). Characteristics that may
allow such control are complex and often idiosyncratic
(some are delineated by Liebold 1989, Strong 1992,
Elser et al. 1996, Polis and Strong 1996, Polis et al.
1996, Power et al. 1996. Brett and Muller-Navara 1997,
Liebold et al. 1997). Overall, these include behavioral
and life history factors that allow efficient and rapid
numerical and functional responses to changes in re-
source abundance and a penchant to eat the dominant
species. Further, it appears that only some plant species
and life stages can be regulated effectively by consump-
tion (e.g., palatable vs noxious algae or forbs, edible
saplings vs lignified trees). Characteristics that align
plants along a vulnerable to resistant axis include chem-
ical and structural defenses, nutrient content. duration
of vulnerable stages, and the reproductive capacity to
dominate a system (Liebold 1989, Strong 1992, Polis
and Strong 1996, Liebold et al. 1997). Overall, it ap-
pears that the strong consumption required to initiate
cascades can occur only with certain combinations of
efficient consumers and vulnerable but productive
plants.
3. Multichannel omnivory and subsidized
consumers
The structure of complex natural systems allows a
subset of those consumers with appropriate life history
traits to become, on occasion, strong top-down forces.
Specifically. consumers that exert strong cascading ef-
fects within a particular plant-herbivore food chain are
almost always deeply subsidized by resources from
many sources or "channels" outside this focal chain.
This is one major point made by Polis and Strong
(1996, see their Fig. 3). "Multichannel" resources in-
clude prey from the detrital channel (Polis 1991a, Polis
and Strong 1996), "spatial subsidies" of prey from
other places (Polis et al. 1997a, b), "temporal subsidies"
of food from previous pulses of productivity (Polis et
al. 1996). and omnivory on other local resources or
foods acquired during other life stages (Polis 1984,
Polis et al. 1996).
Multichannel resources greatly alter interactions in a
focal consumer-resource food chain (Polis and Strong
1996, Polis et al. 1996). They either keep populations of
key consumers stable or present in the system and,or
allow them to occur at high numbers. Multichannel
subsidies produce more consumers than can be sup-
ported by current and local resource productivity.
These consumers then depress their resources. I suggest
that such processes likely underlie most (all?) strong
consumer-resource interactions in natural systems. Sub-
sidies that empowers key consumers are also an essen-
tial component in all community-level trophic cascades
documented to date (Polis and Strong 1996, Polis et al.
1997a, b).
Such multichannel facilitation of cascades does not
conform to the mechanisms subsuming GWH or EEH
theories of consumer control which fixate on processes
within the focal plant-herbivore-predator chain.
N o t all trophic cascades conform to green
world processes
Here, I evaluate two lines of evidence used to support
GWH and EEH theory.
1. Cascades involving subsets of the community
It is important to distinguish two types of cascades:
"species cascades" occur to a subset of the community
whereby changes in predator numbers affect the success
of one or a few plant species; and "community-level
cascades" whereby the distribution of plant biomass
changes substantially throughout an entire system.
Note that all documented cascades on land and many
in water are "species-" and not "community-level" -
they do not explain habitat wide changes in biomass
distribution between plants and animals, as posited by
G W H and EEH theory. They focus on some compo-
nent of a system (usually, one plant species) rather than
the entire community.
Community-level cascades only occur when that
plant species is a particularly dominant component of a
system, as is the case for subtidal kelp (Estes et al.
1998) or stream algae (Power 1990). In all other cases,
species-level trophic cascades have little to do with
community-level dynamics or biomass patterns. More-
over, in many cases, the response by plants to predator
manipulations is statistically rather than biologically
significant (in the sense of producing a substantial
change in plant biomass or productivity). It is not
surprising that reducing predation on herbivores often
allows herbivores to eat more plants - indeed, herbi-
vores are one of the multiple contributing factors that
set plant biomass - but other factors normally stop
herbivores from decimating or even regulating plant
biomass. Thus, to provide evidence for their expanded
green world hypothesis, Hairston and Hairston (1997)
cited the cascade of Spiller and Schoener (1996),
whereby removal of lizards allowed more herbivores
who then increased plant damage. Yet, plant damage
was minimal (a few more leaves were scarred), and the
experimental islands remained quite green as very little
plant biomass was affected.
Thus, the spate of recent studies demonstrating spe-
cies cascades d o not provide the appropriate data to
evaluate if G W H or EEH processes determine commu-
nity patterns of biomass (e.g., Polis and Hurd 1996,
Spiller and Schoener 1996, Moran and Hurd 1998,
Schmitz 1998) (reviewed by Menge 1995, Hairston and
Hairston 1997, Letourneau and Dyer 1998, Persson
1999, Schmitz et al. unpubl.). These studies have little
bearing on the dynamics or structure of whole systems.
Most cascades, including all on land, do not show a
system-wide switch between green and barren. GWH or
EEH try to explain patterns of ecosystem- and habitat-
wide biomass (Liebold et al. 1997).
2. Cascades involving pathogens
Pathogenslparasites (P/P) occasionally suppress herbi-
vores and allow greater plant biomass. Most cited is the
rhinderpest epizootic that devastated ungulates in East
Africa, thus relaxing herbivory and facilitating plant
and tree recruitment (Sinclair 1979). (To me, this is the
only community-level cascade documented on land.)
However, disease outbreaks are always sporadic and
relatively rare, although PlP are virtually everywhere
and host densities may be high for years. These obser-
vations suggest that: P/P are normally rather ineffectual
regulators of herbivore biomass; and P I P abundance is
not a tight function of resource abundance. Why? Most
likely, P/P are held in check by the same types of
factors that control herbivores and other consumers
(Polis and Strong 1996): resource defenses (host immu-
nity), abiotic factors (temperature and desiccation sensi-
tivity), self-regulatory mechanisms, relative resource
shortages (Andrewartha and Birch 1954, White 1978),
and spatial and temporal heterogeneity that make it
difficult to infect hosts.
Moreover, neither mechanisms nor biomass patterns
conform to G W H or EEH theory. In all epizootics,
very little biomass is transferred up to the next "trophic
level" (Polis and Strong 1996). Thus all rhinderpest
viral biomass from thousands of square kilometers of
ungulate destruction would fit in a wine bottle (A.
Dobson pers. comm). So, P I P may be keystone species
(sensu Power et al. 1996) that exert stronger effects than
their biomass would predict, but they are not model
green world agents. Moreover, note that no higher
green world "trophic level" controls most P I P (includ-
ing those that devastate herbivores or plants).
Differences in consumer control between
water and land
Several lines of evidence show that aquatic consumers
are a more influential determinant of standing biomass
(SB) patterns than their terrestrial counterparts: they
take - 3-5 times more ANPP (Table 1); SB:ANPP
ratios are four orders of magnitude higher in terrestrial
environments (Table 1); these ratios and inverted
biomass pyramids show that consumers monopolize
much more plant productivity in water than on land; all
well documented community-level trophic cascades are
aquatic (Strong 1992); and a meta-analysis of lake
cascades (Brett and Goldman 1996) show that they
occur with some frequency; with the exception of rhin-
derpest, little evidence suggests that community-wide
cascades ever occur on land (species cascades do occur).
Why is consumer control of biomass apparently more
important in aquatic systems? Several have considered
this question (e.g., Strong 1992, Carpenter et al. 1992,
Cyr and Pace 1993, Hairston and Hairston 1993, Power
et al. 1996, Liebold et al. 1997). Here is my overview.
1) Plant defrnses - aquatic plants possess less structural
material because buoyancy alleviates the need for
strong skeletons. Most water and land plants have
chemical defenses, but recalcitrant lignin and cellulose
are absent or less concentrated in the algae that domi-
nate aquatic systems. Such skeletons allow aquatic her-
bivores to digest at a faster rate and kill the entire
plant.
2) Size escapes - buoyancy requirements (e.g., high
area,volume ratios) generally constrain key open water
plants and herbivores to be small, and thus, more-or-
less equally vulnerable throughout their existence.
Thus, aquatic consumers generally eat (kill) the entire
plant rather than taking a portion of a land plant.
Large land plants are usually vulnerable only from seed
to sapling, becoming lignified and inedible as they
grow. Multi-year seed production by long-lived land
plants allows successful pulses of recruitment during
good times or when other factors suppress herbivores.
Such regular escapes allow high plant biomass in many
terrestrial systems.
3) Nutrient dynamics - nutrients become available to
aquatic plants at a faster rate than on land because they
recycle and redistribute faster. Thus aquatic plants can
gain nutrients at a fast enough rate to sustain high
levels of productivity which turnover to high levels of
animal biomass. Several factors are involved (2, 4-8).
4) Differences in rates of consurrzption - on average,
rates of herbivory are three times greater in water
versus land. This difference occurs because herbivores
graze more per unit of their biomass in aquatic versus
terrestrial systems (Cyr and Pace 1993). Cyr and Pace
also provide evidence that suggests that predation rates
on herbivores are higher in water versus land. Such
higher rates recycle limiting nutrients more rapidly to
producers and thus perpetuate high levels of consump-
tion in water compared to land.
5) Llfe cycles - key aquatic plants and herbivores
complete their life cycles more quickly because they are
smaller than their terrestrial counterparts. Thus, herbi-
vores show a more efficient numerical response to
increases in plant productivity. Moreover, they die
("turnover") faster. making sequestered nutrients avail-
able to plants sooner. Finally, small organisms have
larger area/volume ratios and consequent greater loss
of dissolved nutrients via cell leakage compared to large
land plants.
6) Excretory products aquatic organisms excrete N in
- 3) Productivity is likewise quite variable in time, e.g.,
a more usable form to plants (i.e., Crustacea ammonia
or fish tri-methy amine oxide vs insect uric acid or
mammalian urea).
7) Nutrient redistribution - water movement (currents,
upwelling, turnover), diffusion, and mobile aquatic con-
sumers redistribute nutrients from rich areas (e.g.. ben-
thic sediment) to plants more thoroughly and rapidly
than physical processes homogenize soil nutrients (nu-
trient distribution is notoriously heterogeneous on land,
Huston 1993).
8) Food web structure - aquatic systems where cascades
occur appear dominated by a few key species of plants
and consumers tightly linked in a linear food chain (see
section Why do trophic cascades occur?). Terrestrial
webs apparently lack such key species or. perhaps, they
are functionally more diverse and reticulate (Strong
1992).
9) Abiotic harshness - drought and temperature ex-
tremes act to reduce the abundance and population
growth rates of consumers in many terrestrial commu-
nities. This slows their numerical response to increased
productivity and allows plants to escape to high num-
12
bers or to resistant sizes. Although many exceptions
occur (e.g., seasonal streams; lakes that freeze or go
anoxic). aquatic systems are generally more benign and
stable: water is usually available and water's high heat
capacity greatly dampens thermal extremes.
Under-appreciated issues
The debate over green world and exploitation ecosys-
tem hypotheses has greatly advanced our scope of food
webs and communities (also see Persson 1999). How-
ever, Ecology should look forward to new frontiers, not
back. Here I identify relatively under-studied areas that
I perceive are central to understanding populations,
food webs, communities, and ecosystems.
1) Populations and food webs are greatly affected by
ecosystem-level processes that determine the production
and use of energy and nutrients. Although logistics and
classical training usually restrict our research to a set of
taxa in particular habitats at certain spatial and tempo-
ral scales, deeper understanding will emerge only when
effective bridges link and integrate traditionally sepa-
rate disciplines. We need to understand how population
dynamics affect ecosystem processes and vice versa
(Jones and Lawton 1995).
2) Great spatial heterogeneity exists and nutrients
and organisms ubiquitously move among habitats to
exert substantial effects (Polis et al. 1997a, b, Huxel and
McCann 1998). How d o spatially variable productivity
and flux of trophic entities affect populations and com-
munities (Polis and Power in press)?
among seasons and years. How does past productivity,
stored and used, affect current interactions (Polis et al.
1996, Polis et al. in press)?
4) Almost all species display complex life cycles,
marked by moderate to radical changes in diet and
habitat: such life histories fundamentally must affect
every species with which they interact (Ebenman and
Persson 1988). Yet. our understanding of how age and
stage structured processes affect food webs and com-
munities is embryonic.
5 ) Most primary productivity is uneaten by herbivores
(median > 80% on land. - 50%) in water). Uneaten
plants (and animals) enter the detrital web where they
are processed by microbes and some metazoa. What
happens to this dominant chunk of the world's produc-
tivity (Wiegert and Owen 1971, DeAngelis 1992, Polis
and Strong 1996)? Is the detrital web a self-contained
sink internally recycling energy and nutrients or a link
that affects the population dynamics of the larger spe-
cies studied by most readers of Oikos? In either case,
we should understand much more about this most
fundamental component of communities.
OIKOS 86 1 (1999)
Overview
A few general questions dominate much of Ecology:
why are there so many different species? What deter-
mines the distribution and abundance of species? What
determines productivity and the distribution of biomass
between plants and consumers? Single factors are often
quite important determinants of abundance, distribu-
tion, diversity. and productivity; however, under other
conditions, they become less significant and other fac-
tors assume more importance. Moreover, they never
operate alone. A major goal is to delineate these fac-
tors; when and where each assumes importance; what
are their relative contributions in a particular system;
what explains their varying strength; and how they vary
and interact. I strongly advocate that, in our quest to
understand and generalize. we use a pluralistic ap-
proach and integrate the richness of natural systems to
produce a satisfying and reasonably realistic view of
how nature operates.
Productivity and biomass distribution are a function
of many factors. They vary because habitats and time
periods differ markedly in precipitation, incident light,
temperature, disturbance, nutrients, resistance to her-
bivory, indirect effects (e.g., mutualism), and cascading
food-web effects. We should approach our research
from a statistical perspective and model productivity or
biomass as a dependent factor whose variance is "ex-
plained" by a number of independent factors. In my
assessment, nutrients and abiotic factors each explain a
very high percentage of variation. Plant defenses ex-
plain another sizeable percentage. Herbivory con-
tributes, on occasion. to explain a substantial fraction
of the variance in productivity and biomass in some
communities (e.g., in many aquatic systems) but con-
tributes much less in other communities (e.g., many
land systems). Green world and exploitation ecosystem
predation on herbivores is demonstrably important in
many aquatic systems, although it is unclear if such
forces dominate most aquatic systems. Cascading pre-
dation appears to explain only a very small fraction of
the variance in the temporal and spatial distribution of
plant biomass in land comn~unities.In some times and
places, each of these factors can ascend to become a
major determinant or may contribute little, especially
relative to other factors. I stress that such pluralistic
thinking should be the core of any conceptual basis to
explain patterns of productivity and biomass distribu-
tion as well as any of the other key issues in ecology.
Acknon~ledgen~ents Many people continue to influence my
-
thinking as I wrestle to understand how nature works; these
include Mary Power, Don Strong. Wendy Anderson, Lennart
Persson, Mike Vanni. Bob Holt, Bruce Menge, Alan Hastings.
Lauri Oksanen, and Janne Bengtsson. Suggestions by April
Boulton, Tom Fenchel. Gary Huxel, Kevin McCann. Lennart
Persson, Francisco Sanchez Piiiero. Paul Stapp, Anna Sears
and Gary Sprules' graduate seminar at University of Toronto
clarified my thinking and writing. This overview presents my
perspective on several issues. I have no doubt whatsoever that
relevant citations and even important ideas are omitted. For
this I apologize.
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